diff --git a/changes/2442.feature.rst b/changes/2442.feature.rst
new file mode 100644
index 000000000..36974d860
--- /dev/null
+++ b/changes/2442.feature.rst
@@ -0,0 +1 @@
+Update Briefcase’s build system to support GUI toolkit-owned pyscript/backend configuration and insertion content.
diff --git a/docs/reference/platforms/web/static.rst b/docs/reference/platforms/web/static.rst
index 7bc9cdc7e..df81cd2cf 100644
--- a/docs/reference/platforms/web/static.rst
+++ b/docs/reference/platforms/web/static.rst
@@ -97,3 +97,45 @@ and change the default PyScript app name, you could use::
     [[runtimes]]
     src = "https://example.com/custom/pyodide.js"
     """
+
+Deployment Configuration
+========================
+
+Web packages can include deployment configuration to control how Briefcase builds
+and deploys web applications.  The deployment process relies on a ``config.toml``
+file and associated deployment files included in Python packages.
+
+config.toml
+-----------
+
+A package can specify deployment settings through a ``config.toml`` file located
+at ``<package>/deploy/config.toml``. The deployment configuration file accepts the
+following information:
+
+* ``implementation``: The web implementation to use (currently only ``"pyscript"``
+  is supported). If not specified, defaults to ``"pyscript"``.
+* ``pyscript.version``: The PyScript version to use (e.g., ``"2024.11.1"``). If not
+  specified, Briefcase will use its default PyScript version.
+
+Example ``config.toml``::
+
+    implementation = "pyscript"
+
+    [pyscript]
+    version = "2024.11.1"
+
+pyscript.toml
+-------------
+
+A package can include a base ``pyscript.toml`` file located at
+``<package>/deploy/pyscript.toml``. The base configuration in this file serves as
+the foundation for Briefcase to generate the final ``pyscript.toml`` file.
+Briefcase performs the following operations when processing this file:
+
+1. The system reads the base ``pyscript.toml`` file from the package directory.
+2. The system adds the ``packages`` list which contains all wheel files to the configuration.
+3. Merge in any :attr:`extra_pyscript_toml_content` from ``pyproject.toml``
+
+A Briefcase project must have only one package that defines deployment configuration
+through a ``config.toml`` file. The system will produce an error when multiple packages
+in the dependencies attempt to define deployment settings.
diff --git a/src/briefcase/platforms/web/static.py b/src/briefcase/platforms/web/static.py
index 88af70717..a7ee828a4 100644
--- a/src/briefcase/platforms/web/static.py
+++ b/src/briefcase/platforms/web/static.py
@@ -1,9 +1,11 @@
 import errno
+import re
 import subprocess
 import sys
 import webbrowser
 from http.server import SimpleHTTPRequestHandler, ThreadingHTTPServer
 from pathlib import Path
+from textwrap import dedent, indent
 from typing import Any
 from zipfile import ZipFile
 
@@ -33,6 +35,21 @@
 )
 from briefcase.config import AppConfig
 
+# Banner templates (Constants used in write_inserts)
+HTML_BANNER = (
+    "<!--------------------------------------------------\n"
+    " * {package}\n"
+    " -------------------------------------------------->\n"
+    "{content}"
+)
+
+CSS_BANNER = (
+    "/**************************************************\n"
+    " * {package}\n"
+    " *************************************************/\n"
+    "{content}"
+)
+
 
 class StaticWebMixin:
     output_format = "static"
@@ -45,8 +62,11 @@ def project_path(self, app):
     def binary_path(self, app):
         return self.bundle_path(app) / "www/index.html"
 
+    def static_path(self, app):
+        return self.project_path(app) / "static"
+
     def wheel_path(self, app):
-        return self.project_path(app) / "static/wheels"
+        return self.static_path(app) / "wheels"
 
     def distribution_path(self, app):
         return self.dist_path / f"{app.formal_name}-{app.version}.web.zip"
@@ -73,56 +93,359 @@ class StaticWebOpenCommand(StaticWebMixin, OpenCommand):
 class StaticWebBuildCommand(StaticWebMixin, BuildCommand):
     description = "Build a static web project."
 
-    def _trim_file(self, path, sentinel):
-        """Re-write a file to strip any content after a sentinel line.
+    def write_inserts(
+        self,
+        app: AppConfig,
+        filename: Path,
+        inserts: dict[str, dict[str, str]],
+    ):
+        """Write inserts into an existing file.
+
+        This function looks for start and end markers in the named file and
+        replaces the content inside the markers with the inserted content.
+
+        Multiple formats of insert marker are inspected to accommodate HTML
+        and CSS/JS comment conventions:
+        * HTML: `<!--@@ insert:start @@--> and <!--@@ insert:end @@-->`
+        * CSS/JS: `/*@@ insert:start @@*/ and /*@@ insert:end @@*/`
 
-        The file is stored in-memory, so it shouldn't be used on files with a *lot* of
-        content before the sentinel.
+        Inserts and package contributions are processed in sorted order to ensure
+        deterministic builds.
 
-        :param path: The path to the file to be trimmed
-        :param sentinel: The content of the sentinel line. This will become the last
-            line in the trimmed file.
+        :param app: The application whose `pyscript.toml` is being written.
+        :param filename: The file whose insert is to be written.
+        :param inserts: The inserts for the file. A 2 level dictionary, keyed by
+            the name of the insert to add, and then package that contributed the
+            insert.
         """
-        content = []
-        with path.open("r", encoding="utf-8") as f:
-            for line in f:
-                if line.rstrip("\n") == sentinel:
-                    content.append(line)
-                    break
-                else:
-                    content.append(line)
+        # Load file content, skip if file not found
+        target_path = self.project_path(app) / filename
+        try:
+            file_text = target_path.read_text(encoding="utf-8")
+        except FileNotFoundError:
+            self.console.warning(f"  Target {filename} not found; skipping inserts.")
+            return
+
+        # Each insert slot and its package contributions are processed in sorted order
+        for insert, pkg_contribs in sorted(inserts.items()):
+            # Build bodies from the same contributions
+            html_body = "\n".join(
+                HTML_BANNER.format(package=pkg, content=text)
+                for pkg, text in sorted(pkg_contribs.items())
+                if text
+            )
+            css_body = "\n".join(
+                CSS_BANNER.format(package=pkg, content=text)
+                for pkg, text in sorted(pkg_contribs.items())
+                if text
+            )
+            body_map = {"html": html_body, "css": css_body}
+
+            slot = re.escape(insert)
+
+            # Build the compiled patterns directly once per slot
+            compiled_markers = [
+                (
+                    re.compile(
+                        rf"(^[ \t]*)<!--@@ {slot}:start @@-->.*?<!--@@ {slot}:end @@-->",
+                        flags=re.MULTILINE | re.DOTALL,
+                    ),
+                    r"{indent}<!--@@ {insert}:start @@-->\n{content}{indent}<!--@@ {insert}:end @@-->",
+                    "html",
+                ),
+                (
+                    re.compile(
+                        rf"(^[ \t]*)/\*@@ {slot}:start @@\*/.*?/\*@@ {slot}:end @@\*/",
+                        flags=re.MULTILINE | re.DOTALL,
+                    ),
+                    r"{indent}/*@@ {insert}:start @@*/\n{content}{indent}/*@@ {insert}:end @@*/",
+                    "css",
+                ),
+            ]
+
+            # Apply all matching marker styles
+            any_match = False
+            for pattern, repl_tmpl, kind in compiled_markers:
+                # Search for pattern within file.
+                pattern_found = pattern.search(file_text)
+                if pattern_found:
+                    # Indent content to align with markers.
+                    indented_content = indent(
+                        body_map.get(kind, "").strip("\n") + "\n",
+                        pattern_found.group(1),
+                    )
+                    file_text = pattern.sub(
+                        repl_tmpl.format(
+                            indent=pattern_found.group(1),
+                            insert=insert,
+                            content=indented_content,
+                        ),
+                        file_text,
+                    )
+                    any_match = True
+
+            if not any_match:
+                self.console.warning(
+                    f"  Slot '{insert}' markers not found in {filename}; skipping."
+                )
+
+        # Save modified content
+        target_path.write_text(file_text, encoding="utf-8")
 
-        with path.open("w", encoding="utf-8") as f:
-            for line in content:
-                f.write(line)
+    def _append_pyscript_insert(
+        self,
+        app: AppConfig,
+        filename: Path,
+        pyscript_version: str,
+        inserts: dict[str, dict[str, dict[str, str]]],
+    ):
+        """Write pyscript version into an existing html file.
 
-    def _process_wheel(self, wheelfile, css_file):
-        """Process a wheel, extracting any content that needs to be compiled into the
-        final project.
+        This function creates an insert for PyScript.
 
-        :param wheelfile: The path to the wheel file to be processed.
-        :param css_file: A file handle, opened for write/append, to which any extracted
-            CSS content will be appended.
+        :param app: The application whose html file is being written.
+        :param filename: The html file whose pyscript version is to be written.
+        :param pyscript_version: The pyscript version number to be inserted.
+        :param inserts: Nested dict of inserts keyed by target - insert - package.
         """
-        package = " ".join(wheelfile.name.split("-")[:2])
+        package_key = "briefcase"
+        target = filename
+        head_insert = "head-python"
+        body_insert = "body-python"
+
+        # PyScript definitions for insertion:
+        head_content = dedent(
+            f"""\
+            <script type="module">
+                // Hide the splash screen when the page is ready.
+                import {{ hooks }} from "https://pyscript.net/releases/{pyscript_version}/core.js";
+                hooks.main.onReady.add(() => {{
+                    document.getElementById("briefcase-splash").classList.add("hidden");
+                }});
+            </script>
+
+            <link rel="stylesheet" href="https://pyscript.net/releases/{pyscript_version}/core.css">
+            <script type="module" src="https://pyscript.net/releases/{pyscript_version}/core.js"></script>
+            """
+        )
+        body_content = dedent(
+            f"""\
+            <script type="py" async="false" config="pyscript.toml">
+                import runpy
+                result = runpy.run_module(
+                    "{app.app_name}", run_name="__main__", alter_sys=True
+                )
+            </script>
+            """
+        )
+
+        pkg_map_head = inserts.setdefault(target, {}).setdefault(head_insert, {})
+        pkg_map_head[package_key] = head_content
+
+        pkg_map_body = inserts.setdefault(target, {}).setdefault(body_insert, {})
+        pkg_map_body[package_key] = body_content
+
+    def _handle_legacy_css(
+        self,
+        wheel: ZipFile,
+        path: Path,
+        filename: str,
+        package_key: str,
+        inserts: dict[str, dict[str, dict[str, str]]],
+    ) -> None:
+        """Handle legacy CSS under /static/*.css and add to briefcase.css.
+
+        Emits a deprecation warning for every legacy CSS file discovered.
+
+        :param wheel: Open wheel ZipFile being processed.
+        :param path: Path object of the file inside the wheel.
+        :param filename: Filename string inside the wheel.
+        :param package_key: Provenance label (e.g. "name version").
+        :param inserts: Nested dict of inserts keyed by target - insert - package.
+        """
+        # Warn on every legacy usage
+        self.console.warning(
+            f"    {Path(wheel.filename).name}: legacy '/static' CSS file {filename} detected.\n"
+            "     Static file handling has been deprecated; this file should be "
+            "converted into an insert."
+        )
+
+        css_text = wheel.read(filename).decode("utf-8")
+
+        rel_inside = "/".join(path.parts[2:])
+        contrib_key = f"{package_key} (legacy static CSS: {rel_inside})"
+
+        # Add CSS content to briefcase.css insert slot
+        target = "static/css/briefcase.css"
+        insert = "css"
+        pkg_map = inserts.setdefault(target, {}).setdefault(insert, {})
+        if contrib_key in pkg_map and pkg_map[contrib_key]:
+            pkg_map[contrib_key] += "\n" + css_text
+        else:
+            pkg_map[contrib_key] = css_text
+
+    def _handle_insert(
+        self,
+        wheel: ZipFile,
+        parts: tuple[str, ...],
+        filename: str,
+        package_key: str,
+        inserts: dict[str, dict[str, dict[str, str]]],
+    ) -> None:
+        """Handle deploy/inserts/<target>~<insert> files and register inserts.
+
+        :param wheel: Open wheel ZipFile being processed.
+        :param parts: Path parts of the filename inside the wheel.
+        :param filename: Filename string inside the wheel.
+        :param package_key: Provenance label (e.g. "name version").
+        :param inserts: Nested dict of inserts keyed by target - insert - package.
+        """
+        self.console.info(f"    Found {filename}")
+
+        rel_inside = "/".join(parts[3:])
+
+        if not rel_inside or rel_inside.endswith("/"):
+            self.console.warning(
+                f"    {filename}: skipping; not a valid insert file (empty path or directory)."
+            )
+            return
+
+        if "~" not in rel_inside:
+            self.console.warning(
+                f"    {filename}: skipping; filename must match '<target>~<insert>'."
+            )
+            return
+
+        # Preserve any '~' that might exist in the target path by splitting from the right
+        target, insert = rel_inside.rsplit("~", 1)
+        self.console.info(f"    {filename}: Adding {insert} insert for {target}")
+
+        text = wheel.read(filename).decode("utf-8")
+
+        contrib_key = f"{package_key} (deploy insert: {rel_inside} from {filename})"
+        pkg_map = inserts.setdefault(target, {}).setdefault(insert, {})
+        if contrib_key in pkg_map and pkg_map[contrib_key]:
+            pkg_map[contrib_key] += "\n" + text
+        else:
+            pkg_map[contrib_key] = text
+
+    def _process_wheel(
+        self,
+        wheelfile,
+        inserts: dict[str, dict[str, dict[str, str]]],
+    ) -> None:
+        """Process a wheel to collect insert and style content.
+
+        Scans the wheel for:
+        * Legacy CSS - .css files under /static/ added to briefcase.css.
+        * Deploy inserts - files under /deploy/inserts/<target>~<insert>.
+
+        :param wheelfile: Path to the wheel file.
+        :param inserts: Nested dict of inserts keyed by target - insert - package.
+        """
+        name_parts = wheelfile.name.split("-")
+        package_key = f"{name_parts[0]} {name_parts[1]}"
+
         with ZipFile(wheelfile) as wheel:
-            for filename in wheel.namelist():
+            for filename in sorted(wheel.namelist()):
+                # Skip directories and shallow paths
                 path = Path(filename)
-                # Any CSS file in a `static` folder is appended
+                parts = path.parts
+
+                # Legacy CSS handling
                 if (
-                    len(path.parts) > 1
-                    and path.parts[1] == "static"
-                    and path.suffix == ".css"
+                    len(parts) > 1
+                    and parts[1] == "static"
+                    and path.suffix.lower() == ".css"
                 ):
-                    self.console.info(f"    Found {filename}")
-                    css_file.write(
-                        "\n/*******************************************************\n"
+                    self._handle_legacy_css(wheel, path, filename, package_key, inserts)
+
+                # New deploy/inserts handling
+                elif len(parts) >= 3 and parts[1] == "deploy" and parts[2] == "inserts":
+                    self._handle_insert(wheel, parts, filename, package_key, inserts)
+
+    def extract_pyscript_config(self, wheels):
+        """Process multiple wheels to gather a config.toml and a base pyscript.toml
+        file.
+
+        :param wheels: A list of wheel files to be scanned.
+        """
+        config_package = None
+        config_package_list = []
+        config_filename = None
+        pyscript_version = "2024.11.1"
+        pyscript_config = None
+
+        # Find packages containing a config.toml file.
+        for wheelfile in wheels:
+            with ZipFile(wheelfile) as wheel:
+                for filename in wheel.namelist():
+                    path = Path(filename)
+                    if (
+                        len(path.parts) == 3
+                        and path.parts[1] == "deploy"
+                        and path.name == "config.toml"
+                    ):
+                        self.console.info(f"    Found {filename}")
+                        config_package_list.append(wheelfile)
+                        config_filename = filename
+
+        # Return a blank pyscript config if no configuration file is found.
+        if len(config_package_list) == 0:
+            pyscript_config = {}
+        # Raise an error if more than one configuration file is supplied.
+        elif len(config_package_list) > 1:
+            raise BriefcaseConfigError(
+                "Only one deployment configuration file can be supplied. "
+                f"Initial config.toml found in package: {config_package}; "
+                f"Duplicate config.toml found in package: {wheel.filename}"
+            )
+        # Gather a deployment configuration file from the package. For now, this is a
+        # pyscript.toml as no other backend is currently supported.
+        else:
+            with (
+                ZipFile(config_package_list[0]) as wheel,
+                wheel.open(config_filename) as config_file,
+            ):
+                config_data = tomllib.load(config_file)
+
+                # Gather implementation from config.toml
+                implementation = config_data.get("implementation", None)
+
+                # Currently, only pyscript is supported. Warn if another implementation is found,
+                # but fail safe to using pyscript with a warning.
+                if implementation is None:
+                    self.console.warning(
+                        "No web implementation specified. Defaulting to 'pyscript'."
                     )
-                    css_file.write(f" * {package}::{'/'.join(path.parts[2:])}\n")
-                    css_file.write(
-                        " *******************************************************/\n\n"
+                elif implementation != "pyscript":
+                    self.console.warning(
+                        "At present, 'pyscript' is the only supported web implementation. "
+                        "This project may not work correctly."
                     )
-                    css_file.write(wheel.read(filename).decode("utf-8"))
+
+                # Get pyscript version from config.toml. Use default if not present.
+                pyscript_version = config_data.get("pyscript", {}).get(
+                    "version", pyscript_version
+                )
+
+                # Extract pyscript.toml
+                pyscript_path = config_filename.replace("config.toml", "pyscript.toml")
+                try:
+                    with wheel.open(pyscript_path) as pyscript_file:
+                        pyscript_config = tomllib.load(pyscript_file)
+                except tomllib.TOMLDecodeError as e:
+                    raise BriefcaseConfigError(
+                        f"pyscript.toml content isn't valid TOML: {e}"
+                    ) from e
+                except (KeyError, FileNotFoundError):
+                    self.console.info(
+                        f"Pyscript configuration file not found in {config_package_list[0]}. "
+                        "Using default configuration."
+                    )
+                    pyscript_config = {}
+
+        return pyscript_config, pyscript_version
 
     def build_app(self, app: AppConfig, **kwargs):
         """Build the static web deployment for the application.
@@ -186,17 +509,11 @@ def build_app(self, app: AppConfig, **kwargs):
                 ) from e
 
         with self.console.wait_bar("Writing Pyscript configuration file..."):
-            # Load any pre-existing pyscript.toml provided by the template. If the file
+            # Load any pre-existing pyscript.toml provided by a GUI Toolkit. If the file
             # doesn't exist, assume an empty pyscript.toml as a starting point.
-            try:
-                with (self.project_path(app) / "pyscript.toml").open("rb") as f:
-                    config = tomllib.load(f)
-            except tomllib.TOMLDecodeError as e:
-                raise BriefcaseConfigError(
-                    f"pyscript.toml content isn't valid TOML: {e}"
-                ) from e
-            except FileNotFoundError:
-                config = {}
+            config, pyscript_version = self.extract_pyscript_config(
+                self.wheel_path(app).glob("*.whl")
+            )
 
             # Add the packages declaration to the existing pyscript.toml.
             # Ensure that we're using Unix path separators, as the content
@@ -218,24 +535,26 @@ def build_app(self, app: AppConfig, **kwargs):
             except AttributeError:
                 pass
 
-            # Write the final configuration.
+            # Write the final configuration
             with (self.project_path(app) / "pyscript.toml").open("wb") as f:
                 tomli_w.dump(config, f)
 
-        self.console.info("Compile static web content from wheels")
         with self.console.wait_bar("Compiling static web content from wheels..."):
-            # Trim previously compiled content out of briefcase.css
-            briefcase_css_path = self.project_path(app) / "static/css/briefcase.css"
-            self._trim_file(
-                briefcase_css_path,
-                sentinel=" ******************* Wheel contributed styles **********************/",
-            )
+            inserts: dict[str, dict[str, dict[str, str]]] = {}
 
-            # Extract static resources from packaged wheels
             for wheelfile in sorted(self.wheel_path(app).glob("*.whl")):
                 self.console.info(f"  Processing {wheelfile.name}...")
-                with briefcase_css_path.open("a", encoding="utf-8") as css_file:
-                    self._process_wheel(wheelfile, css_file=css_file)
+                self._process_wheel(
+                    wheelfile=wheelfile,
+                    inserts=inserts,
+                )
+
+            # Add pyscript insertion to inserts
+            self._append_pyscript_insert(app, "index.html", pyscript_version, inserts)
+
+            # Write inserts per target
+            for target, target_inserts in sorted(inserts.items()):
+                self.write_inserts(app, Path(target), target_inserts)
 
         return {}
 
diff --git a/tests/platforms/web/static/conftest.py b/tests/platforms/web/static/conftest.py
index d71fd25d4..fa2d14153 100644
--- a/tests/platforms/web/static/conftest.py
+++ b/tests/platforms/web/static/conftest.py
@@ -16,19 +16,34 @@ def first_app_generated(first_app_config, tmp_path):
 """,
     )
 
-    # Create index.html
-    create_file(bundle_path / "www/index.html", "<html></html>")
-
-    # Create the initial pyscript.toml
+    # Create index.html with insert markers
     create_file(
-        bundle_path / "www/pyscript.toml",
-        """
-existing-key-1 = "value-1"
-existing-key-2 = 2
+        bundle_path / "www/index.html",
+        """<!doctype html>
+<html>
+  <head>
+    <!--@@ head:start @@-->
+    <!--@@ head:end @@-->
+    <!--@@ head-python:start @@-->
+    <!--@@ head-python:end @@-->
+  </head>
+  <body>
+    <div id="briefcase-splash"></div>
+
+    <!--@@ body-start:start @@-->
+    <!--@@ body-start:end @@-->
+
+    <!--@@ body-python:start @@-->
+    <!--@@ body-python:end @@-->
+
+    <!--@@ body-end:start @@-->
+    <!--@@ body-end:end @@-->
+  </body>
+</html>
 """,
     )
 
-    # Create the initial briefcase.css
+    # Create the initial briefcase.css with CSS insert markers
     create_file(
         bundle_path / "www/static/css/briefcase.css",
         """
@@ -36,7 +51,10 @@ def first_app_generated(first_app_config, tmp_path):
   display: None;
 }
 /*******************************************************************
- ******************** Wheel contributed styles ********************/
+******************** Wheel contributed styles ********************/
+/*@@ css:start @@*/
+/*@@ css:end @@*/
+
 """,
     )
 
@@ -50,12 +68,6 @@ def first_app_generated(first_app_config, tmp_path):
 def first_app_built(first_app_generated, tmp_path):
     bundle_path = tmp_path / "base_path/build/first-app/web/static"
 
-    # Create pyscript.toml
-    create_file(
-        bundle_path / "www/pyscript.toml",
-        'packages = ["dummy-1.2.3-py3-none-all.whl"]',
-    )
-
     # Create an app wheel
     create_wheel(bundle_path / "www/static/wheels")
 
diff --git a/tests/platforms/web/static/test_build.py b/tests/platforms/web/static/test_build.py
index 3838d92c9..f34b0a696 100644
--- a/tests/platforms/web/static/test_build.py
+++ b/tests/platforms/web/static/test_build.py
@@ -15,7 +15,7 @@
 from briefcase.integrations.subprocess import Subprocess
 from briefcase.platforms.web.static import StaticWebBuildCommand
 
-from ....utils import create_file, create_wheel
+from ....utils import create_wheel
 
 
 @pytest.fixture
@@ -47,6 +47,22 @@ def mock_run(*args, **kwargs):
                 "first_app",
                 extra_content=[
                     ("dependency/static/style.css", "span { margin: 10px; }\n"),
+                    (
+                        "dependency/deploy/config.toml",
+                        """
+implementation = "pyscript"
+
+[pyscript]
+version = "2024.11.1"
+""",
+                    ),
+                    (
+                        "dependency/deploy/pyscript.toml",
+                        """
+existing-key-1 = "value-1"
+existing-key-2 = 2
+""",
+                    ),
                 ],
             )
         elif args[0][5] == "pip":
@@ -132,6 +148,60 @@ def mock_run(*args, **kwargs):
             ],
         }
 
+    # index.html has insertions
+    with (bundle_path / "www/index.html").open(encoding="utf-8") as f:
+        assert (
+            f.read()
+            == "\n".join(
+                [
+                    "<!doctype html>",
+                    "<html>",
+                    "  <head>",
+                    "    <!--@@ head:start @@-->",
+                    "    <!--@@ head:end @@-->",
+                    "    <!--@@ head-python:start @@-->",
+                    "    <!--------------------------------------------------",
+                    "     * briefcase",
+                    "     -------------------------------------------------->",
+                    '    <script type="module">',
+                    "        // Hide the splash screen when the page is ready.",
+                    '        import { hooks } from "https://pyscript.net/releases/2024.11.1/core.js";',
+                    "        hooks.main.onReady.add(() => {",
+                    '            document.getElementById("briefcase-splash").classList.add("hidden");',
+                    "        });",
+                    "    </script>",
+                    "",
+                    '    <link rel="stylesheet" href="https://pyscript.net/releases/2024.11.1/core.css">',
+                    '    <script type="module" src="https://pyscript.net/releases/2024.11.1/core.js"></script>',
+                    "    <!--@@ head-python:end @@-->",
+                    "  </head>",
+                    "  <body>",
+                    '    <div id="briefcase-splash"></div>',
+                    "",
+                    "    <!--@@ body-start:start @@-->",
+                    "    <!--@@ body-start:end @@-->",
+                    "",
+                    "    <!--@@ body-python:start @@-->",
+                    "    <!--------------------------------------------------",
+                    "     * briefcase",
+                    "     -------------------------------------------------->",
+                    '    <script type="py" async="false" config="pyscript.toml">',
+                    "        import runpy",
+                    "        result = runpy.run_module(",
+                    '            "first-app", run_name="__main__", alter_sys=True',
+                    "        )",
+                    "    </script>",
+                    "    <!--@@ body-python:end @@-->",
+                    "",
+                    "    <!--@@ body-end:start @@-->",
+                    "    <!--@@ body-end:end @@-->",
+                    "  </body>",
+                    "</html>",
+                ]
+            )
+            + "\n"
+        )
+
     # briefcase.css has been appended
     with (bundle_path / "www/static/css/briefcase.css").open(encoding="utf-8") as f:
         assert (
@@ -143,25 +213,24 @@ def mock_run(*args, **kwargs):
                     "  display: None;",
                     "}",
                     "/*******************************************************************",
-                    " ******************** Wheel contributed styles ********************/",
-                    "",
-                    "/*******************************************************",
-                    " * dependency 1.2.3::style.css",
-                    " *******************************************************/",
-                    "",
+                    "******************** Wheel contributed styles ********************/",
+                    "/*@@ css:start @@*/",
+                    "/**************************************************",
+                    " * dependency 1.2.3 (legacy static CSS: style.css)",
+                    " *************************************************/",
                     "div { margin: 10px; }",
                     "",
-                    "/*******************************************************",
-                    " * first_app 1.2.3::style.css",
-                    " *******************************************************/",
-                    "",
+                    "/**************************************************",
+                    " * first_app 1.2.3 (legacy static CSS: style.css)",
+                    " *************************************************/",
                     "span { margin: 10px; }",
                     "",
-                    "/*******************************************************",
-                    " * other 1.2.3::style.css",
-                    " *******************************************************/",
-                    "",
+                    "/**************************************************",
+                    " * other 1.2.3 (legacy static CSS: style.css)",
+                    " *************************************************/",
                     "div { padding: 10px; }",
+                    "/*@@ css:end @@*/",
+                    "",
                 ]
             )
             + "\n"
@@ -195,6 +264,12 @@ def test_build_app_custom_pyscript_toml(build_command, first_app_generated, tmp_
         bundle_path / "www/static/wheels"
     )
 
+    # Mock extracting pyscript.toml from a wheel.
+    build_command.extract_pyscript_config = lambda _: (
+        {"existing-key-1": "value-1", "existing-key-2": 2},
+        "2024.11.1",
+    )
+
     # Build the web app.
     build_command.build_app(first_app_generated)
 
@@ -212,56 +287,6 @@ def test_build_app_custom_pyscript_toml(build_command, first_app_generated, tmp_
         }
 
 
-def test_build_app_no_template_pyscript_toml(
-    build_command, first_app_generated, tmp_path
-):
-    """An app whose template doesn't provide pyscript.toml gets a basic config."""
-    # Remove the templated pyscript.toml
-    bundle_path = tmp_path / "base_path/build/first-app/web/static"
-    (bundle_path / "www/pyscript.toml").unlink()
-
-    # Mock the side effect of invoking shutil
-    build_command.tools.shutil.rmtree.side_effect = lambda *args: shutil.rmtree(
-        bundle_path / "www/static/wheels"
-    )
-
-    # Build the web app.
-    build_command.build_app(first_app_generated)
-
-    # Pyscript.toml has been written with only the packages content
-    with (bundle_path / "www/pyscript.toml").open("rb") as f:
-        assert tomllib.load(f) == {
-            "packages": [],
-        }
-
-
-def test_build_app_invalid_template_pyscript_toml(
-    build_command, first_app_generated, tmp_path
-):
-    """An app with an invalid pyscript.toml raises an error."""
-    # Re-write an invalid templated pyscript.toml
-    bundle_path = tmp_path / "base_path/build/first-app/web/static"
-    (bundle_path / "www/pyscript.toml").unlink()
-    create_file(
-        bundle_path / "www/pyscript.toml",
-        """
-This is not valid toml.
-""",
-    )
-
-    # Mock the side effect of invoking shutil
-    build_command.tools.shutil.rmtree.side_effect = lambda *args: shutil.rmtree(
-        bundle_path / "www/static/wheels"
-    )
-
-    # Building the web app raises an error
-    with pytest.raises(
-        BriefcaseConfigError,
-        match=r"Briefcase configuration error: pyscript.toml content isn't valid TOML: Expected",
-    ):
-        build_command.build_app(first_app_generated)
-
-
 def test_build_app_invalid_extra_pyscript_toml_content(
     build_command, first_app_generated, tmp_path
 ):
@@ -370,6 +395,12 @@ def mock_run(*args, **kwargs):
         bundle_path / "www/static/wheels"
     )
 
+    # Mock extracting pyscript.toml from a wheel.
+    build_command.extract_pyscript_config = lambda _: (
+        {"existing-key-1": "value-1", "existing-key-2": 2},
+        "2024.11.1",
+    )
+
     # Build the web app.
     build_command.build_app(first_app_generated)
 
@@ -436,13 +467,14 @@ def mock_run(*args, **kwargs):
                     "  display: None;",
                     "}",
                     "/*******************************************************************",
-                    " ******************** Wheel contributed styles ********************/",
-                    "",
-                    "/*******************************************************",
-                    " * first_app 1.2.3::style.css",
-                    " *******************************************************/",
-                    "",
+                    "******************** Wheel contributed styles ********************/",
+                    "/*@@ css:start @@*/",
+                    "/**************************************************",
+                    " * first_app 1.2.3 (legacy static CSS: style.css)",
+                    " *************************************************/",
                     "span { margin: 10px; }",
+                    "/*@@ css:end @@*/",
+                    "",
                 ]
             )
             + "\n"
@@ -499,13 +531,6 @@ def test_app_package_fail(build_command, first_app_generated, tmp_path):
     # Wheels folder still exists
     assert (bundle_path / "www/static/wheels").is_dir()
 
-    # Pyscript.toml content has not changed
-    with (bundle_path / "www/pyscript.toml").open("rb") as f:
-        assert tomllib.load(f) == {
-            "existing-key-1": "value-1",
-            "existing-key-2": 2,
-        }
-
 
 def test_dependency_fail(build_command, first_app_generated, tmp_path):
     """If dependencies can't be downloaded, an error is raised."""
@@ -574,10 +599,3 @@ def test_dependency_fail(build_command, first_app_generated, tmp_path):
 
     # Wheels folder still exists
     assert (bundle_path / "www/static/wheels").is_dir()
-
-    # Pyscript.toml content has not changed
-    with (bundle_path / "www/pyscript.toml").open("rb") as f:
-        assert tomllib.load(f) == {
-            "existing-key-1": "value-1",
-            "existing-key-2": 2,
-        }
diff --git a/tests/platforms/web/static/test_build__handle_insert.py b/tests/platforms/web/static/test_build__handle_insert.py
new file mode 100644
index 000000000..aaf6c4bd0
--- /dev/null
+++ b/tests/platforms/web/static/test_build__handle_insert.py
@@ -0,0 +1,168 @@
+import zipfile
+from pathlib import Path
+
+import pytest
+
+from briefcase.platforms.web.static import StaticWebBuildCommand
+
+
+@pytest.fixture
+def build_command(dummy_console, tmp_path):
+    return StaticWebBuildCommand(
+        console=dummy_console,
+        base_path=tmp_path / "base_path",
+        data_path=tmp_path / "briefcase",
+    )
+
+
+def test_handle_insert_register_valid_file(build_command, tmp_path):
+    """Valid insert is registered under target/slot."""
+    wheel_path = Path(tmp_path) / "dummy-1.2.3.whl"
+    filename = "dummy/deploy/inserts/index.html~header"
+    with zipfile.ZipFile(wheel_path, "w") as zf:
+        zf.writestr(filename, "<s>ok</s>")
+
+    inserts = {}
+    with zipfile.ZipFile(wheel_path) as zf:
+        build_command._handle_insert(
+            wheel=zf,
+            parts=Path(filename).parts,
+            filename=filename,
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
+
+    assert "index.html" in inserts and "header" in inserts["index.html"]
+    assert any("<s>ok</s>" in v for v in inserts["index.html"]["header"].values())
+
+
+@pytest.mark.parametrize(
+    "entry, expected_skip",
+    [
+        ("dummy/deploy/inserts/", True),  # Top-level directory entry
+        ("dummy/deploy/inserts/assets/", False),  # Nested directory entry
+    ],
+)
+def test_handle_insert_skip_dir_entries(
+    build_command,
+    tmp_path,
+    capsys,
+    entry,
+    expected_skip,
+):
+    """Deploy/inserts directory entries are skipped with a debug log.
+
+    Parametrised: runs once for top-level dir and once for nested dir.
+    """
+    # Create a dummy wheel containing the "directory" entry
+    wheel_path = Path(tmp_path) / "dummy-1.2.3.whl"
+    with zipfile.ZipFile(wheel_path, "w") as zf:
+        zf.writestr(entry, "")
+
+    # Run the handler against this entry
+    inserts = {}
+    with zipfile.ZipFile(wheel_path) as zf:
+        build_command._handle_insert(
+            wheel=zf,
+            parts=Path(entry).parts,
+            filename=entry,
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
+
+    output = capsys.readouterr().out
+
+    # Directory entries should be ignored completely
+    assert inserts == {}
+    # And a debug message explaining the skip should be logged
+    if expected_skip:
+        assert "skipping; not a valid insert file" in output
+    else:
+        assert "skipping; not a valid insert file" not in output
+
+
+def test_handle_insert_missing_tilde_skipped(
+    build_command,
+    tmp_path,
+    capsys,
+):
+    """Files under deploy/inserts without '~' are skipped with a debug log."""
+    # Create a dummy wheel containing an invalid insert file (no "~" in name)
+    wheel_filename = Path(tmp_path) / "dummy-1.2.3.whl"
+    missing_tilde = "dummy/deploy/inserts/index.html"
+    with zipfile.ZipFile(wheel_filename, "w") as zf:
+        zf.writestr(missing_tilde, "<div>oops</div>")
+
+    inserts = {}
+    # Run handler directly on the invalid file
+    with zipfile.ZipFile(wheel_filename) as zf:
+        build_command._handle_insert(
+            wheel=zf,
+            parts=Path(missing_tilde).parts,
+            filename=missing_tilde,
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
+
+    output = capsys.readouterr().out
+
+    # File should be ignored completely
+    assert inserts == {}
+    # And a debug message should clearly say why (missing "~")
+    assert "must match '<target>~<insert>'" in output
+
+
+def test_handle_insert_append_existing_contrib(build_command, tmp_path):
+    """Second insert with same contrib key appends with newline."""
+    wheel_path = Path(tmp_path) / "dummy-1.2.3.whl"
+    filename = "dummy/deploy/inserts/index.html~header"
+    with zipfile.ZipFile(wheel_path, "w") as zf:
+        zf.writestr(filename, "<first/>")
+
+    inserts = {}
+    # First registration creates contrib entry
+    with zipfile.ZipFile(wheel_path) as zf:
+        build_command._handle_insert(
+            wheel=zf,
+            parts=Path(filename).parts,
+            filename=filename,
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
+        # Second registration appends to same key
+        build_command._handle_insert(
+            wheel=zf,
+            parts=Path(filename).parts,
+            filename=filename,
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
+
+    contribs = inserts["index.html"]["header"]
+    contrib_key = next(iter(contribs.keys()))
+    value = contribs[contrib_key]
+
+    assert value.count("<first/>") == 2
+    assert "\n" in value
+
+
+def test_handle_insert_non_utf8_raises(
+    build_command,
+    tmp_path,
+):
+    """Non-UTF8 insert content raises UnicodeDecodeError."""
+    bad = b"\xff\xfe\xfa"
+    wheel_path = Path(tmp_path) / "dummy-1.2.3.whl"
+    filename = "dummy/deploy/inserts/index.html~header"
+    with zipfile.ZipFile(wheel_path, "w") as zf:
+        zf.writestr(filename, bad)
+
+    inserts = {}
+    with zipfile.ZipFile(wheel_path) as zf, pytest.raises(UnicodeDecodeError):
+        build_command._handle_insert(
+            wheel=zf,
+            parts=Path(filename).parts,
+            filename=filename,
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
diff --git a/tests/platforms/web/static/test_build__handle_legacy_css.py b/tests/platforms/web/static/test_build__handle_legacy_css.py
new file mode 100644
index 000000000..d90b3e107
--- /dev/null
+++ b/tests/platforms/web/static/test_build__handle_legacy_css.py
@@ -0,0 +1,80 @@
+import zipfile
+from pathlib import Path
+
+import pytest
+
+from briefcase.platforms.web.static import StaticWebBuildCommand
+
+
+@pytest.fixture
+def build_command(dummy_console, tmp_path):
+    return StaticWebBuildCommand(
+        console=dummy_console,
+        base_path=tmp_path / "base_path",
+        data_path=tmp_path / "briefcase",
+    )
+
+
+def test_handle_legacy_css_warn_and_append(
+    build_command,
+    tmp_path,
+    capsys,
+):
+    """Legacy CSS warns and appends to new contrib key."""
+    wheel_path = Path(tmp_path) / "dummy-1.2.3.whl"
+    with zipfile.ZipFile(wheel_path, "w") as zf:
+        zf.writestr("dummy/static/one.css", "h1 { x:1; }")
+
+    inserts = {}
+    with zipfile.ZipFile(wheel_path) as zf:
+        # First call - warn
+        build_command._handle_legacy_css(
+            wheel=zf,
+            path=Path("dummy/static/one.css"),
+            filename="dummy/static/one.css",
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
+        # Pre-seed same contrib key to force append on second call
+        target_map = inserts.setdefault("static/css/briefcase.css", {}).setdefault(
+            "css", {}
+        )
+        key = "pkg 1.0 (legacy static CSS: one.css)"
+        target_map[key] = target_map[key] + "\n/*extra*/"
+        # Second call - no additional warning, content appended
+        build_command._handle_legacy_css(
+            wheel=zf,
+            path=Path("dummy/static/one.css"),
+            filename="dummy/static/one.css",
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
+
+    # One warning for each file
+    output = capsys.readouterr().out
+    assert (
+        "dummy-1.2.3.whl: legacy '/static' CSS file dummy/static/one.css detected."
+        in output
+    )
+
+    # Content appended
+    out = inserts["static/css/briefcase.css"]["css"][key]
+    assert "h1 { x:1; }" in out and "/*extra*/" in out
+
+
+def test_handle_legacy_css_non_utf8_raise(build_command, tmp_path):
+    """Non-UTF8 legacy CSS raises an UnicodeDecodeError."""
+    bad = b"\xff\xfe\xfa"
+    wheel_path = Path(tmp_path) / "dummy-1.2.3.whl"
+    with zipfile.ZipFile(wheel_path, "w") as zf:
+        zf.writestr("dummy/static/bad.css", bad)
+
+    inserts = {}
+    with zipfile.ZipFile(wheel_path) as zf, pytest.raises(UnicodeDecodeError):
+        build_command._handle_legacy_css(
+            wheel=zf,
+            path=Path("dummy/static/bad.css"),
+            filename="dummy/static/bad.css",
+            package_key="pkg 1.0",
+            inserts=inserts,
+        )
diff --git a/tests/platforms/web/static/test_build__process_wheel.py b/tests/platforms/web/static/test_build__process_wheel.py
index 91482bb58..af135e1f1 100644
--- a/tests/platforms/web/static/test_build__process_wheel.py
+++ b/tests/platforms/web/static/test_build__process_wheel.py
@@ -1,5 +1,3 @@
-from io import StringIO
-
 import pytest
 
 from briefcase.platforms.web.static import StaticWebBuildCommand
@@ -19,63 +17,51 @@ def build_command(dummy_console, tmp_path):
 def test_process_wheel(build_command, tmp_path):
     """A wheel can be processed to have CSS content extracted."""
 
-    # Create a wheel with some content.
+    # Create a wheel with some content
     wheel_filename = create_wheel(
         tmp_path,
         extra_content=[
-            # Two CSS files
+            # Three CSS files
             (
                 "dummy/static/first.css",
                 "span {\n  font-color: red;\n  font-size: larger\n}\n",
             ),
-            ("dummy/static/second.css", "div {\n  padding: 10px\n}\n"),
-            ("dummy/static/deep/third.css", "p {\n  color: red\n}\n"),
+            (
+                "dummy/static/second.css",
+                "div {\n  padding: 10px\n}\n",
+            ),
+            (
+                "dummy/static/deep/third.css",
+                "p {\n  color: red\n}\n",
+            ),
             # Content in the static file that isn't CSS
             ("dummy/static/explosions.js", "alert('boom!');"),
-            # CSS in a location that isn't the static folder.
+            # CSS in a location that isn't the static folder
             ("dummy/other.css", "div.other {\n  margin: 10px\n}\n"),
             ("lost.css", "div.lost {\n  margin: 10px\n}\n"),
         ],
     )
 
-    # Create a dummy css file
-    css_file = StringIO()
-
-    build_command._process_wheel(wheel_filename, css_file=css_file)
-
-    assert (
-        css_file.getvalue()
-        == "\n".join(
-            [
-                "",
-                "/*******************************************************",
-                " * dummy 1.2.3::first.css",
-                " *******************************************************/",
-                "",
-                "span {",
-                "  font-color: red;",
-                "  font-size: larger",
-                "}",
-                "",
-                "/*******************************************************",
-                " * dummy 1.2.3::second.css",
-                " *******************************************************/",
-                "",
-                "div {",
-                "  padding: 10px",
-                "}",
-                "",
-                "/*******************************************************",
-                " * dummy 1.2.3::deep/third.css",
-                " *******************************************************/",
-                "",
-                "p {",
-                "  color: red",
-                "}",
-            ]
-        )
-        + "\n"
-    )
+    # Collect into inserts dict
+    inserts = {}
+    build_command._process_wheel(wheelfile=wheel_filename, inserts=inserts)
+
+    # Legacy CSS should be collected into the briefcase.css "css" insert slot
+    assert inserts == {
+        "static/css/briefcase.css": {
+            "css": {
+                "dummy 1.2.3 (legacy static CSS: first.css)": (
+                    "span {\n  font-color: red;\n  font-size: larger\n}\n"
+                ),
+                "dummy 1.2.3 (legacy static CSS: second.css)": (
+                    "div {\n  padding: 10px\n}\n"
+                ),
+                "dummy 1.2.3 (legacy static CSS: deep/third.css)": (
+                    "p {\n  color: red\n}\n"
+                ),
+            }
+        }
+    }
 
 
 def test_process_wheel_no_content(build_command, tmp_path):
@@ -93,9 +79,60 @@ def test_process_wheel_no_content(build_command, tmp_path):
         ],
     )
 
-    # Create a dummy css file
-    css_file = StringIO()
+    inserts = {}
+    build_command._process_wheel(wheelfile=wheel_filename, inserts=inserts)
+
+    assert inserts == {}
+
+
+def test_process_wheel_deploy_inserts(build_command, tmp_path):
+    """Deploy inserts are collected into the correct insert slot."""
+    wheel_filename = create_wheel(
+        tmp_path,
+        extra_content=[
+            ("dummy/deploy/inserts/index.html~header", "<script>alert('hi')</script>"),
+            (
+                "dummy/deploy/inserts/static/css/briefcase.css~CSS",
+                "body { margin: 0; }",
+            ),
+        ],
+    )
+
+    inserts = {}
+    build_command._process_wheel(wheelfile=wheel_filename, inserts=inserts)
+
+    # The index.html header insert exists
+    assert "index.html" in inserts
+    assert "header" in inserts["index.html"]
+    contribs = inserts["index.html"]["header"]
+    assert any("<script>" in v for v in contribs.values())
 
-    build_command._process_wheel(wheel_filename, css_file=css_file)
+    # The CSS insert exists
+    assert "static/css/briefcase.css" in inserts
+    assert "CSS" in inserts["static/css/briefcase.css"]
+    css_contribs = inserts["static/css/briefcase.css"]["CSS"]
+    assert any("body { margin: 0; }" in v for v in css_contribs.values())
 
-    assert css_file.getvalue() == ""
+
+def test_process_wheel_legacy_css_warn_once(build_command, tmp_path, capsys):
+    """Legacy CSS files trigger a single deprecation warning."""
+    wheel_filename = create_wheel(
+        tmp_path,
+        extra_content=[
+            ("dummy/static/one.css", "h1 { color: blue; }"),
+            ("dummy/static/two.css", "h2 { color: green; }"),
+        ],
+    )
+
+    inserts = {}
+    build_command._process_wheel(wheelfile=wheel_filename, inserts=inserts)
+
+    output = capsys.readouterr().out
+    assert (
+        "dummy-1.2.3-py3-none-any.whl: legacy '/static' CSS file dummy/static/one.css detected."
+        in output
+    )
+    assert (
+        "dummy-1.2.3-py3-none-any.whl: legacy '/static' CSS file dummy/static/two.css detected."
+        in output
+    )
diff --git a/tests/platforms/web/static/test_build__trim_file.py b/tests/platforms/web/static/test_build__trim_file.py
deleted file mode 100644
index fbb92b382..000000000
--- a/tests/platforms/web/static/test_build__trim_file.py
+++ /dev/null
@@ -1,118 +0,0 @@
-import pytest
-
-from briefcase.platforms.web.static import StaticWebBuildCommand
-
-from ....utils import create_file
-
-
-@pytest.fixture
-def build_command(dummy_console, tmp_path):
-    return StaticWebBuildCommand(
-        console=dummy_console,
-        base_path=tmp_path / "base_path",
-        data_path=tmp_path / "briefcase",
-    )
-
-
-def test_trim_file(build_command, tmp_path):
-    """A file can be trimmed at a sentinel."""
-    filename = tmp_path / "dummy.txt"
-    content = [
-        "This is before the sentinel.",
-        "This is also before the sentinel.",
-        " ** This is the sentinel ** ",
-        "This is after the sentinel.",
-        "This is also after the sentinel.",
-    ]
-
-    create_file(filename, "\n".join(content))
-
-    # Trim the file at the sentinel
-    build_command._trim_file(filename, sentinel=" ** This is the sentinel ** ")
-
-    # The file contains everything up to and including the sentinel.
-    with filename.open(encoding="utf-8") as f:
-        assert f.read() == "\n".join(content[:3]) + "\n"
-
-
-def test_trim_no_sentinel(build_command, tmp_path):
-    """A file that doesn't contain the sentinel is returned as-is."""
-    filename = tmp_path / "dummy.txt"
-    content = [
-        "This is before the sentinel.",
-        "This is also before the sentinel.",
-        "NO SENTINEL HERE",
-        "This is after the sentinel.",
-        "This is also after the sentinel.",
-    ]
-
-    create_file(filename, "\n".join(content))
-
-    # Trim the file at a sentinel
-    build_command._trim_file(filename, sentinel=" ** This is the sentinel ** ")
-
-    # The file is unmodified.
-    with filename.open(encoding="utf-8") as f:
-        assert f.read() == "\n".join(content)
-
-
-def test_trim_file_multiple_sentinels(build_command, tmp_path):
-    """A file with multiple sentinels is trimmed at the first one."""
-    filename = tmp_path / "dummy.txt"
-    content = [
-        "This is before the sentinel.",
-        "This is also before the sentinel.",
-        " ** This is the sentinel ** ",
-        "This is after the first sentinel.",
-        "This is also after the first sentinel.",
-        " ** This is the sentinel ** ",
-        "This is after the second sentinel.",
-        "This is also after the second sentinel.",
-    ]
-
-    create_file(filename, "\n".join(content))
-
-    # Trim the file at the sentinel
-    build_command._trim_file(filename, sentinel=" ** This is the sentinel ** ")
-
-    # The file contains everything up to and including the sentinel.
-    with filename.open(encoding="utf-8") as f:
-        assert f.read() == "\n".join(content[:3]) + "\n"
-
-
-def test_trim_sentinel_last_line(build_command, tmp_path):
-    """A file with the sentinel as the last full line isn't a problem."""
-    filename = tmp_path / "dummy.txt"
-    content = [
-        "This is before the sentinel.",
-        "This is also before the sentinel.",
-        " ** This is the sentinel ** ",
-    ]
-
-    create_file(filename, "\n".join(content) + "\n")
-
-    # Trim the file at a sentinel
-    build_command._trim_file(filename, sentinel=" ** This is the sentinel ** ")
-
-    # The file is unmodified.
-    with filename.open(encoding="utf-8") as f:
-        assert f.read() == "\n".join(content) + "\n"
-
-
-def test_trim_sentinel_EOF(build_command, tmp_path):
-    """A file with the sentinel at EOF isn't a problem."""
-    filename = tmp_path / "dummy.txt"
-    content = [
-        "This is before the sentinel.",
-        "This is also before the sentinel.",
-        " ** This is the sentinel ** ",
-    ]
-
-    create_file(filename, "\n".join(content))
-
-    # Trim the file at a sentinel
-    build_command._trim_file(filename, sentinel=" ** This is the sentinel ** ")
-
-    # The file is unmodified.
-    with filename.open(encoding="utf-8") as f:
-        assert f.read() == "\n".join(content)
diff --git a/tests/platforms/web/static/test_build_extract_pyscript_config.py b/tests/platforms/web/static/test_build_extract_pyscript_config.py
new file mode 100644
index 000000000..8eb51a2d3
--- /dev/null
+++ b/tests/platforms/web/static/test_build_extract_pyscript_config.py
@@ -0,0 +1,225 @@
+import shutil
+import sys
+from unittest import mock
+
+if sys.version_info >= (3, 11):  # pragma: no-cover-if-lt-py311
+    pass
+else:  # pragma: no-cover-if-gte-py311
+    pass
+
+from zipfile import ZipFile
+
+import pytest
+
+from briefcase.exceptions import BriefcaseConfigError
+from briefcase.integrations.subprocess import Subprocess
+from briefcase.platforms.web.static import StaticWebBuildCommand
+
+
+@pytest.fixture
+def build_command(dummy_console, tmp_path):
+    command = StaticWebBuildCommand(
+        console=dummy_console,
+        base_path=tmp_path / "base_path",
+        data_path=tmp_path / "briefcase",
+    )
+    command.tools.subprocess = mock.MagicMock(spec_set=Subprocess)
+    command.tools.shutil = mock.MagicMock(spec_set=shutil)
+
+    return command
+
+
+def _mock_wheel(tmp_path, wheel_name, files):
+    """Function to mock wheel files in tests."""
+    wheel_path = tmp_path / wheel_name
+    with ZipFile(wheel_path, "w") as wheel:
+        for filename, content in files.items():
+            wheel.writestr(filename, content)
+    return wheel_path
+
+
+def test_extract_pyscript_config(build_command, tmp_path):
+    """Test function works correctly with both config.toml and pyscript.toml."""
+    # Mock a wheel with files
+    files = {
+        "dependency/deploy/config.toml": """
+implementation = "pyscript"
+
+[pyscript]
+version = "2024.10.1"
+""",
+        "dependency/deploy/pyscript.toml": """
+existing-key-1 = "value-1"
+existing-key-2 = 2
+""",
+    }
+
+    wheel_path = _mock_wheel(tmp_path=tmp_path, wheel_name="dependency", files=files)
+
+    # Run the function.
+    pyscript_config, pyscript_version = build_command.extract_pyscript_config(
+        [wheel_path]
+    )
+
+    # Check returns are correct and files were found.
+    assert pyscript_config == {
+        "existing-key-1": "value-1",
+        "existing-key-2": 2,
+    }
+    assert pyscript_version == "2024.10.1"
+
+
+def test_extract_pyscript_config_no_config(build_command, tmp_path):
+    """If no config.toml supplied by wheels, functions returns a basic config."""
+    # Mock a wheel without the needed files
+    files = {"dependency/deploy/not-the-files-you-are-looking-for.toml": ""}
+
+    wheel_path = _mock_wheel(tmp_path=tmp_path, wheel_name="dependency", files=files)
+
+    # Run the function.
+    pyscript_config, pyscript_version = build_command.extract_pyscript_config(
+        [wheel_path]
+    )
+
+    # Check pyscript_config is empty and pyscript_version is the default.
+    assert pyscript_config == {}
+    assert pyscript_version == "2024.11.1"
+
+
+def test_extract_pyscript_config_multiple_config(build_command, tmp_path):
+    """Multiple config.toml supplied by wheels fails."""
+
+    # Mock wheels that both contain config.toml
+    file_set_1 = {
+        "dependency/deploy/config.toml": """
+implementation = "pyscript"
+
+[pyscript]
+version = "2024.10.1"
+""",
+    }
+
+    file_set_2 = {
+        "dependency/deploy/config.toml": """
+implementation = "pyscript"
+
+[pyscript]
+version = "2024.10.1"
+""",
+    }
+
+    wheel_path_1 = _mock_wheel(
+        tmp_path=tmp_path, wheel_name="dependency", files=file_set_1
+    )
+    wheel_path_2 = _mock_wheel(
+        tmp_path=tmp_path, wheel_name="dependency", files=file_set_2
+    )
+
+    # Run the function.
+    with pytest.raises(
+        BriefcaseConfigError,
+        match=r"Only one deployment configuration file can be supplied.",
+    ):
+        build_command.extract_pyscript_config([wheel_path_1, wheel_path_2])
+
+
+def test_extract_pyscript_config_no_implementation(build_command, tmp_path, capsys):
+    """An app with no "implementation" value defaults to pyscript with a warning."""
+
+    # Mock a wheel with the needed files
+    files = {"dependency/deploy/config.toml": ""}
+
+    wheel_path = _mock_wheel(tmp_path=tmp_path, wheel_name="dependency", files=files)
+
+    pyscript_config, pyscript_version = build_command.extract_pyscript_config(
+        [wheel_path]
+    )
+
+    # Capture output and assert warning present.
+    captured = capsys.readouterr()
+    assert "No web implementation specified. Defaulting to 'pyscript'." in captured.out
+
+    # Check pyscript_config is empty and pyscript_version is the default.
+    assert pyscript_config == {}
+    assert pyscript_version == "2024.11.1"
+
+
+def test_extract_pyscript_config_implementation_warning(
+    build_command,
+    tmp_path,
+    capsys,
+):
+    """Briefcase raises a warning if "implementation" value is not pyscript."""
+
+    files = {
+        "dependency/deploy/config.toml": """
+implementation = "something-else"
+""",
+    }
+
+    wheel_path = _mock_wheel(tmp_path=tmp_path, wheel_name="dependency", files=files)
+
+    pyscript_config, pyscript_version = build_command.extract_pyscript_config(
+        [wheel_path]
+    )
+
+    # Capture output and assert warning present.
+    captured = capsys.readouterr()
+    assert (
+        "At present, 'pyscript' is the only supported web implementation."
+        in captured.out
+    )
+
+    # Check pyscript_config is empty and pyscript_version is the default.
+    assert pyscript_config == {}
+    assert pyscript_version == "2024.11.1"
+
+
+def test_extract_pyscript_config_no_pyscript_toml(build_command, tmp_path, capsys):
+    """If no pyscript.toml is supplied by a wheel, function returns a basic config."""
+
+    # Create wheel with no pyscript.toml
+    files = {
+        "dependency/deploy/config.toml": """
+implementation = "pyscript"
+""",
+    }
+
+    wheel_path = _mock_wheel(tmp_path=tmp_path, wheel_name="dependency", files=files)
+
+    pyscript_config, pyscript_version = build_command.extract_pyscript_config(
+        [wheel_path]
+    )
+    # Capture output and assert console info is present.
+    captured = capsys.readouterr()
+    assert "Pyscript configuration file not found in" in captured.out
+
+    # Check pyscript_config is empty and pyscript_version is the default.
+    assert pyscript_config == {}
+    assert pyscript_version == "2024.11.1"
+
+
+def test_extract_pyscript_config_invalid_wheel_pyscript_toml(build_command, tmp_path):
+    """A wheel with an invalid pyscript.toml raises an error."""
+
+    # Mock a wheel with files
+    files = {
+        "dependency/deploy/config.toml": """
+implementation = "pyscript"
+
+[pyscript]
+version = "2024.10.1"
+""",
+        "dependency/deploy/pyscript.toml": """
+This is not valid toml.
+""",
+    }
+
+    wheel_path = _mock_wheel(tmp_path=tmp_path, wheel_name="dependency", files=files)
+
+    # Building the web app raises an error
+    with pytest.raises(
+        BriefcaseConfigError,
+        match=r"Briefcase configuration error: pyscript.toml content isn't valid TOML: Expected",
+    ):
+        build_command.extract_pyscript_config([wheel_path])
diff --git a/tests/platforms/web/static/test_build_write_inserts.py b/tests/platforms/web/static/test_build_write_inserts.py
new file mode 100644
index 000000000..e8a7eb452
--- /dev/null
+++ b/tests/platforms/web/static/test_build_write_inserts.py
@@ -0,0 +1,224 @@
+from pathlib import Path
+from textwrap import dedent
+
+import pytest
+
+from briefcase.console import Console
+from briefcase.platforms.web.static import CSS_BANNER, StaticWebBuildCommand
+
+
+@pytest.fixture
+def build_command(tmp_path):
+    return StaticWebBuildCommand(
+        console=Console(),
+        base_path=tmp_path / "base_path",
+        data_path=tmp_path / "briefcase",
+    )
+
+
+@pytest.fixture
+def app_config(first_app_config, tmp_path):
+    first_app_config._path = tmp_path / "base_path/build/first-app/web/static"
+    (first_app_config._path / "www").mkdir(parents=True)
+    return first_app_config
+
+
+def write_target_file(base_path, rel_filename, content):
+    target = base_path / "www" / rel_filename
+    target.parent.mkdir(parents=True, exist_ok=True)
+    target.write_text(content, encoding="utf-8")
+    return target
+
+
+def test_write_insert_warn_if_slot_missing(build_command, app_config, monkeypatch):
+    """Warn if insert slot markers are missing from the file."""
+
+    # File without insert markers
+    file_text = "<html>No markers here</html>"
+    target = write_target_file(app_config._path, "index.html", file_text)
+
+    # Capture warnings
+    warnings = []
+    monkeypatch.setattr(build_command.console, "warning", warnings.append)
+
+    # Attempt to insert into missing slot
+    inserts = {"header": {"pkg": "<div/>"}}
+    build_command.write_inserts(app_config, Path("index.html"), inserts)
+
+    # Ensure warning was raised and file is unchanged
+    assert any("markers not found" in w for w in warnings)
+    assert target.read_text(encoding="utf-8") == file_text
+
+
+def test_write_insert_warn_if_file_missing(build_command, app_config, monkeypatch):
+    """Warn if the target file does not exist."""
+
+    # Capture warnings
+    warnings = []
+    monkeypatch.setattr(build_command.console, "warning", warnings.append)
+
+    # Attempt to insert into a file that doesn’t exist
+    inserts = {"header": {"pkg": "<div/>"}}
+    build_command.write_inserts(app_config, Path("notexist.html"), inserts)
+
+    # Ensure warning was raised
+    assert any("Target notexist.html not found" in w for w in warnings)
+
+
+def test_write_insert_is_idempotent(build_command, app_config):
+    """Inserts should be idempotent when run multiple times."""
+
+    # File with placeholder slot
+    file_text = dedent(
+        """\
+        <html>
+        <!--@@ header:start @@-->
+        PLACEHOLDER
+        <!--@@ header:end @@-->
+        </html>
+        """
+    )
+    target = write_target_file(app_config._path, "index.html", file_text)
+
+    # Apply insert once
+    inserts = {"header": {"pkg": "<p>Hello</p>"}}
+    build_command.write_inserts(app_config, Path("index.html"), inserts)
+    once = target.read_text(encoding="utf-8")
+
+    # Apply insert again
+    build_command.write_inserts(app_config, Path("index.html"), inserts)
+    twice = target.read_text(encoding="utf-8")
+
+    # Ensure result did not change
+    assert once == twice
+
+
+def test_write_insert_slot_name_regex_escaped(build_command, app_config):
+    """Slots containing regex chars should be escaped and matched literally."""
+
+    # File with marker containing regex chars
+    file_text = dedent(
+        """\
+        <html>
+        <!--@@ head[er]:start @@-->
+        PLACEHOLDER
+        <!--@@ head[er]:end @@-->
+        </html>
+        """
+    )
+    target = write_target_file(app_config._path, "index.html", file_text)
+
+    # Insert into regex-like slot name
+    inserts = {"head[er]": {"pkg": "<p>works</p>"}}
+    build_command.write_inserts(app_config, Path("index.html"), inserts)
+
+    # Ensure content was inserted correctly
+    out = target.read_text(encoding="utf-8")
+    assert "works" in out
+
+
+def test_write_insert_css_packages_sorted(build_command, app_config):
+    """Multiple CSS contributions should be inserted in sorted order."""
+
+    # File with CSS marker slot
+    file_text = "/*@@ css:start @@*/\nold\n/*@@ css:end @@*/\n"
+    target = write_target_file(app_config._path, "static/css/briefcase.css", file_text)
+
+    # Insert two contributions out of order
+    inserts = {"css": {"b": "b{}", "a": "a{}"}}
+    build_command.write_inserts(app_config, Path("static/css/briefcase.css"), inserts)
+
+    out = target.read_text(encoding="utf-8")
+    a_block = CSS_BANNER.format(package="a", content="a{}")
+    b_block = CSS_BANNER.format(package="b", content="b{}")
+
+    # Ensure alphabetical order and removal of old content
+    assert out.index(a_block) < out.index(b_block)
+    assert "old" not in out
+
+
+def test_write_insert_replaces_all_matches(build_command, app_config):
+    """All matching slots should be replaced, not just the first occurrence."""
+
+    # File with two identical slots
+    file_text = (
+        "<!--@@ h:start @@-->X<!--@@ h:end @@-->\n"
+        "<!--@@ h:start @@-->Y<!--@@ h:end @@-->\n"
+    )
+    target = write_target_file(app_config._path, "index.html", file_text)
+
+    # Insert replacement content
+    inserts = {"h": {"pkg": "Z"}}
+    build_command.write_inserts(app_config, Path("index.html"), inserts)
+
+    out = target.read_text(encoding="utf-8")
+
+    # Both occurrences replaced
+    assert "X" not in out and "Y" not in out
+    assert out.count("Z") == 2
+
+
+def test_write_insert_handles_html_and_css_markers(build_command, app_config):
+    """HTML and CSS marker styles should both be processed in one file."""
+
+    # File containing both HTML and CSS markers
+    file_text = dedent("""\
+        <html>
+          <!--@@ assets:start @@-->
+          OLD_HTML
+          <!--@@ assets:end @@-->
+          <style>
+          /*@@ assets:start @@*/
+          OLD_CSS
+          /*@@ assets:end @@*/
+          </style>
+        </html>
+    """)
+    target = write_target_file(app_config._path, "index.html", file_text)
+
+    # Insert HTML and CSS contributions
+    inserts = {"assets": {"pkgA": "<link/>", "pkgB": "h1{}"}}
+    build_command.write_inserts(app_config, Path("index.html"), inserts)
+
+    out = target.read_text(encoding="utf-8")
+
+    # Ensure both banners appear, new content is inserted, and old content removed
+    assert "<!--------------------------------------------------" in out
+    assert "<link/>" in out
+    assert "/**************************************************" in out
+    assert "h1{}" in out
+    assert "OLD_HTML" not in out and "OLD_CSS" not in out
+
+
+def test_write_insert_preserves_multiline_indent(build_command, app_config):
+    """Inserted multiline content should preserve indentation of markers."""
+
+    # File with indented marker slot
+    file_text = "    <!--@@ header:start @@-->\n    X\n    <!--@@ header:end @@-->\n"
+    target = write_target_file(app_config._path, "index.html", file_text)
+
+    # Insert multiline content
+    inserts = {"header": {"pkg": "L1\nL2"}}
+    build_command.write_inserts(app_config, Path("index.html"), inserts)
+
+    out = target.read_text(encoding="utf-8")
+
+    # Ensure inserted lines are indented properly
+    assert "\n    L1\n    L2\n" in out
+
+
+def test_write_insert_ignores_empty_contributions(build_command, app_config):
+    """Empty insert contributions should be ignored (no banner written)."""
+
+    # File with CSS marker slot
+    file_text = "/*@@ css:start @@*/\nX\n/*@@ css:end @@*/\n"
+    target = write_target_file(app_config._path, "static/css/briefcase.css", file_text)
+
+    # Provide empty contribution
+    inserts = {"css": {"pkg": ""}}
+    build_command.write_inserts(app_config, Path("static/css/briefcase.css"), inserts)
+
+    out = target.read_text(encoding="utf-8")
+
+    # Ensure no banner for empty contribution
+    assert " * pkg" not in out
diff --git a/tests/platforms/web/static/test_package.py b/tests/platforms/web/static/test_package.py
index bfe2af07b..66aab995e 100644
--- a/tests/platforms/web/static/test_package.py
+++ b/tests/platforms/web/static/test_package.py
@@ -36,7 +36,6 @@ def test_package_app(package_command, first_app_built, tmp_path):
     with ZipFile(archive_file) as archive:
         assert sorted(archive.namelist()) == [
             "index.html",
-            "pyscript.toml",
             "static/",
             "static/css/",
             "static/css/briefcase.css",