diff --git a/airflow-core/src/airflow/api_fastapi/execution_api/app.py b/airflow-core/src/airflow/api_fastapi/execution_api/app.py
index 449019db7998d..7dcb8951f2699 100644
--- a/airflow-core/src/airflow/api_fastapi/execution_api/app.py
+++ b/airflow-core/src/airflow/api_fastapi/execution_api/app.py
@@ -44,9 +44,12 @@
     get_sig_validation_args,
     get_signing_args,
 )
+from airflow.process_context import override_process_context
 
 if TYPE_CHECKING:
     import httpx
+    from a2wsgi.asgi_typing import ASGIApp as A2WSGIApp
+    from starlette.types import ASGIApp, Receive, Scope, Send
 
 import structlog
 from structlog.contextvars import bind_contextvars
@@ -367,6 +370,17 @@ def _shutdown_loop(
     thread.join(timeout=5)
 
 
+class _RequestScopedServerContextApp:
+    """Wrap an ASGI app so in-process requests behave like server-side API handling."""
+
+    def __init__(self, app: FastAPI) -> None:
+        self.app = app
+
+    async def __call__(self, scope: Scope, receive: Receive, send: Send) -> None:
+        with override_process_context("server"):
+            await self.app(scope, receive, send)
+
+
 @attrs.define()
 class InProcessExecutionAPI:
     """
@@ -376,10 +390,11 @@ class InProcessExecutionAPI:
     needed so that we can use the sync httpx client
     """
 
+    request_scoped_server_context: bool = attrs.field(default=False, kw_only=True)
     _app: FastAPI | None = None
 
     @cached_property
-    def app(self):
+    def app(self) -> FastAPI:
         if not self._app:
             from airflow.api_fastapi.common.dagbag import create_dag_bag
             from airflow.api_fastapi.execution_api.datamodels.token import TIClaims, TIToken
@@ -409,6 +424,12 @@ async def always_allow(request: Request):
 
         return self._app
 
+    @cached_property
+    def asgi_app(self) -> ASGIApp:
+        if self.request_scoped_server_context:
+            return _RequestScopedServerContextApp(self.app)
+        return self.app
+
     @cached_property
     def transport(self) -> httpx.WSGITransport:
         import httpx
@@ -420,7 +441,7 @@ def transport(self) -> httpx.WSGITransport:
         thread = threading.Thread(target=loop.run_forever, name="InProcessExecutionAPI-loop", daemon=True)
         thread.start()
 
-        middleware = ASGIMiddleware(self.app, loop=loop)
+        middleware = ASGIMiddleware(cast("A2WSGIApp", self.asgi_app), loop=loop)
 
         # https://github.com/abersheeran/a2wsgi/discussions/64
         async def start_lifespan(cm: AsyncExitStack, app: FastAPI):
@@ -447,4 +468,4 @@ async def start_lifespan(cm: AsyncExitStack, app: FastAPI):
     def atransport(self) -> httpx.ASGITransport:
         import httpx
 
-        return httpx.ASGITransport(app=self.app)
+        return httpx.ASGITransport(app=self.asgi_app)
diff --git a/airflow-core/src/airflow/models/connection.py b/airflow-core/src/airflow/models/connection.py
index 1b4b0f8f86768..b1ec6beaee562 100644
--- a/airflow-core/src/airflow/models/connection.py
+++ b/airflow-core/src/airflow/models/connection.py
@@ -20,7 +20,6 @@
 import json
 import logging
 import re
-import sys
 import warnings
 from contextlib import suppress
 from json import JSONDecodeError
@@ -50,6 +49,7 @@ class AirflowSecretsBackendAccessDenied(PermissionError):  # type: ignore[no-red
         """Compat stub — never raised by task-sdk <1.2.2."""
 
 
+from airflow.process_context import should_use_task_sdk_api_path
 from airflow.utils.helpers import prune_dict
 from airflow.utils.log.logging_mixin import LoggingMixin
 from airflow.utils.session import NEW_SESSION, provide_session
@@ -475,7 +475,7 @@ def get_connection_from_secrets(cls, conn_id: str, team_name: str | None = None)
 
         # If this is set it means are in some kind of execution context (Task, Dag Parse or Triggerer perhaps)
         # and should use the Task SDK API server path
-        if hasattr(sys.modules.get("airflow.sdk.execution_time.task_runner"), "SUPERVISOR_COMMS"):
+        if should_use_task_sdk_api_path():
             from airflow.sdk import Connection as TaskSDKConnection
             from airflow.sdk.exceptions import AirflowRuntimeError, ErrorType
 
@@ -566,7 +566,7 @@ def to_dict(self, *, prune_empty: bool = False, validate: bool = True) -> dict[s
 
     @classmethod
     def from_json(cls, value, conn_id=None) -> Connection:
-        if hasattr(sys.modules.get("airflow.sdk.execution_time.task_runner"), "SUPERVISOR_COMMS"):
+        if should_use_task_sdk_api_path():
             from airflow.sdk import Connection as TaskSDKConnection
 
             warnings.warn(
diff --git a/airflow-core/src/airflow/models/variable.py b/airflow-core/src/airflow/models/variable.py
index b06e73cd5f50a..f29bdd55fc7eb 100644
--- a/airflow-core/src/airflow/models/variable.py
+++ b/airflow-core/src/airflow/models/variable.py
@@ -20,7 +20,6 @@
 import contextlib
 import json
 import logging
-import sys
 import warnings
 from typing import TYPE_CHECKING, Any
 
@@ -47,6 +46,7 @@ class AirflowSecretsBackendAccessDenied(PermissionError):  # type: ignore[no-red
         """Compat stub — never raised by task-sdk <1.2.2."""
 
 
+from airflow.process_context import should_use_task_sdk_api_path
 from airflow.secrets.metastore import MetastoreBackend
 from airflow.utils.log.logging_mixin import LoggingMixin
 from airflow.utils.session import NEW_SESSION, create_session, provide_session
@@ -166,7 +166,7 @@ def get(
 
         # If this is set it means we are in some kind of execution context (Task, Dag Parse or Triggerer perhaps)
         # and should use the Task SDK API server path
-        if hasattr(sys.modules.get("airflow.sdk.execution_time.task_runner"), "SUPERVISOR_COMMS"):
+        if should_use_task_sdk_api_path():
             warnings.warn(
                 "Using Variable.get from `airflow.models` is deprecated."
                 "Please use `get` on Variable from sdk(`airflow.sdk.Variable`) instead",
@@ -226,7 +226,7 @@ def set(
 
         # If this is set it means we are in some kind of execution context (Task, Dag Parse or Triggerer perhaps)
         # and should use the Task SDK API server path
-        if hasattr(sys.modules.get("airflow.sdk.execution_time.task_runner"), "SUPERVISOR_COMMS"):
+        if should_use_task_sdk_api_path():
             warnings.warn(
                 "Using Variable.set from `airflow.models` is deprecated."
                 "Please use `set` on Variable from sdk(`airflow.sdk.Variable`) instead",
@@ -314,7 +314,7 @@ def update(
 
         # If this is set it means are in some kind of execution context (Task, Dag Parse or Triggerer perhaps)
         # and should use the Task SDK API server path
-        if hasattr(sys.modules.get("airflow.sdk.execution_time.task_runner"), "SUPERVISOR_COMMS"):
+        if should_use_task_sdk_api_path():
             warnings.warn(
                 "Using Variable.update from `airflow.models` is deprecated."
                 "Please use `set` on Variable from sdk(`airflow.sdk.Variable`) instead as it is an upsert.",
@@ -380,7 +380,7 @@ def delete(key: str, team_name: str | None = None, session: Session | None = Non
 
         # If this is set it means are in some kind of execution context (Task, Dag Parse or Triggerer perhaps)
         # and should use the Task SDK API server path
-        if hasattr(sys.modules.get("airflow.sdk.execution_time.task_runner"), "SUPERVISOR_COMMS"):
+        if should_use_task_sdk_api_path():
             warnings.warn(
                 "Using Variable.delete from `airflow.models` is deprecated."
                 "Please use `delete` on Variable from sdk(`airflow.sdk.Variable`) instead",
diff --git a/airflow-core/src/airflow/process_context.py b/airflow-core/src/airflow/process_context.py
new file mode 100644
index 0000000000000..1655d6e81fbb8
--- /dev/null
+++ b/airflow-core/src/airflow/process_context.py
@@ -0,0 +1,59 @@
+# Licensed to the Apache Software Foundation (ASF) under one
+# or more contributor license agreements.  See the NOTICE file
+# distributed with this work for additional information
+# regarding copyright ownership.  The ASF licenses this file
+# to you under the Apache License, Version 2.0 (the
+# "License"); you may not use this file except in compliance
+# with the License.  You may obtain a copy of the License at
+#
+#   http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing,
+# software distributed under the License is distributed on an
+# "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
+# KIND, either express or implied.  See the License for the
+# specific language governing permissions and limitations
+# under the License.
+from __future__ import annotations
+
+import os
+import sys
+from collections.abc import Generator
+from contextlib import contextmanager
+from contextvars import ContextVar
+from typing import Literal
+
+__all__ = [
+    "get_process_context",
+    "override_process_context",
+    "should_use_task_sdk_api_path",
+]
+
+_PROCESS_CONTEXT_OVERRIDE: ContextVar[str | None] = ContextVar(
+    "_AIRFLOW_PROCESS_CONTEXT_OVERRIDE",
+    default=None,
+)
+
+
+def get_process_context() -> str | None:
+    """Return the current process context, preferring request-scoped overrides."""
+    return _PROCESS_CONTEXT_OVERRIDE.get() or os.environ.get("_AIRFLOW_PROCESS_CONTEXT")
+
+
+@contextmanager
+def override_process_context(context: Literal["server", "client"]) -> Generator[None, None, None]:
+    """Temporarily override the current process context for the active execution flow."""
+    token = _PROCESS_CONTEXT_OVERRIDE.set(context)
+    try:
+        yield
+    finally:
+        _PROCESS_CONTEXT_OVERRIDE.reset(token)
+
+
+def should_use_task_sdk_api_path() -> bool:
+    """Return True when execution-context helpers should route through Task SDK APIs."""
+    if get_process_context() == "server":
+        return False
+
+    task_runner_module = sys.modules.get("airflow.sdk.execution_time.task_runner")
+    return bool(getattr(task_runner_module, "SUPERVISOR_COMMS", None))
diff --git a/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_connections.py b/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_connections.py
index a2e3cb51fab32..19e87bafd14c1 100644
--- a/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_connections.py
+++ b/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_connections.py
@@ -17,6 +17,7 @@
 
 from __future__ import annotations
 
+import sys
 from unittest import mock
 
 import pytest
@@ -105,6 +106,40 @@ def test_connection_get_from_env_var(self, client, session):
             "extra": '{"headers": "header"}',
         }
 
+    @mock.patch.dict(
+        "os.environ",
+        {
+            "AIRFLOW_CONN_TEST_CONN_SERVER": '{"uri": "http://root:admin@localhost:8080/https?headers=header"}',
+            "_AIRFLOW_PROCESS_CONTEXT": "server",
+        },
+    )
+    def test_connection_get_uses_server_path_when_supervisor_comms_exists(self, client):
+        fake_task_runner = mock.Mock()
+        fake_task_runner.SUPERVISOR_COMMS = object()
+
+        with (
+            mock.patch.dict(sys.modules, {"airflow.sdk.execution_time.task_runner": fake_task_runner}),
+            mock.patch(
+                "airflow.sdk.Connection.get",
+                side_effect=AssertionError(
+                    "Execution API should not route through Task SDK Connection.get in server context"
+                ),
+            ),
+        ):
+            response = client.get("/execution/connections/test_conn_server")
+
+        assert response.status_code == 200
+        assert response.json() == {
+            "conn_id": "test_conn_server",
+            "conn_type": "http",
+            "host": "localhost",
+            "login": "root",
+            "password": "admin",
+            "schema": "https",
+            "port": 8080,
+            "extra": '{"headers": "header"}',
+        }
+
     def test_connection_get_not_found(self, client):
         response = client.get("/execution/connections/non_existent_test_conn")
 
diff --git a/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_variables.py b/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_variables.py
index f078d6c2fe06f..b5c6c6985fdd6 100644
--- a/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_variables.py
+++ b/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_variables.py
@@ -96,6 +96,28 @@ def test_variable_get_from_env_var(self, client, session):
         assert response.status_code == 200
         assert response.json() == {"key": "key1", "value": "VALUE"}
 
+    @mock.patch.dict(
+        "os.environ",
+        {"AIRFLOW_VAR_KEY1": "VALUE", "_AIRFLOW_PROCESS_CONTEXT": "server"},
+    )
+    def test_variable_get_uses_server_path_when_supervisor_comms_exists(self, client):
+        fake_task_runner = mock.Mock()
+        fake_task_runner.SUPERVISOR_COMMS = object()
+
+        with (
+            mock.patch.dict("sys.modules", {"airflow.sdk.execution_time.task_runner": fake_task_runner}),
+            mock.patch(
+                "airflow.sdk.Variable.get",
+                side_effect=AssertionError(
+                    "Execution API should not route through Task SDK Variable.get in server context"
+                ),
+            ),
+        ):
+            response = client.get("/execution/variables/key1")
+
+        assert response.status_code == 200
+        assert response.json() == {"key": "key1", "value": "VALUE"}
+
     @pytest.mark.parametrize(
         "key",
         [
@@ -158,6 +180,31 @@ def test_should_create_variable(self, client, key, payload, session):
         if "description" in payload:
             assert var_from_db.description == payload["description"]
 
+    @mock.patch.dict(
+        "os.environ",
+        {"_AIRFLOW_PROCESS_CONTEXT": "server"},
+    )
+    def test_variable_put_uses_server_path_when_supervisor_comms_exists(self, client, session):
+        fake_task_runner = mock.Mock()
+        fake_task_runner.SUPERVISOR_COMMS = object()
+
+        with (
+            mock.patch.dict("sys.modules", {"airflow.sdk.execution_time.task_runner": fake_task_runner}),
+            mock.patch(
+                "airflow.sdk.Variable.set",
+                side_effect=AssertionError(
+                    "Execution API should not route through Task SDK Variable.set in server context"
+                ),
+            ),
+        ):
+            response = client.put("/execution/variables/var_server_only", json={"value": "server_value"})
+
+        assert response.status_code == 201
+        assert response.json()["message"] == "Variable successfully set"
+        var_from_db = session.scalars(select(Variable).where(Variable.key == "var_server_only")).first()
+        assert var_from_db is not None
+        assert var_from_db.val == "server_value"
+
     @pytest.mark.parametrize(
         ("key", "payload", "error_type"),
         [
@@ -342,3 +389,29 @@ def test_should_not_delete_variable(self, client, session):
 
         vars = session.scalars(select(Variable)).all()
         assert len(vars) == 1
+
+    @mock.patch.dict(
+        "os.environ",
+        {"_AIRFLOW_PROCESS_CONTEXT": "server"},
+    )
+    def test_variable_delete_uses_server_path_when_supervisor_comms_exists(self, client, session):
+        Variable.set(key="var_server_delete", value="to_delete", session=session)
+        session.commit()
+
+        fake_task_runner = mock.Mock()
+        fake_task_runner.SUPERVISOR_COMMS = object()
+
+        with (
+            mock.patch.dict("sys.modules", {"airflow.sdk.execution_time.task_runner": fake_task_runner}),
+            mock.patch(
+                "airflow.sdk.Variable.delete",
+                side_effect=AssertionError(
+                    "Execution API should not route through Task SDK Variable.delete in server context"
+                ),
+            ),
+        ):
+            response = client.delete("/execution/variables/var_server_delete")
+
+        assert response.status_code == 204
+        session.expire_all()
+        assert session.scalar(select(Variable).where(Variable.key == "var_server_delete")) is None
diff --git a/airflow-core/tests/unit/models/test_connection.py b/airflow-core/tests/unit/models/test_connection.py
index 94cabe5e4daf4..1fd0d755cae7d 100644
--- a/airflow-core/tests/unit/models/test_connection.py
+++ b/airflow-core/tests/unit/models/test_connection.py
@@ -49,6 +49,12 @@ def clear_fernet_cache(self):
         yield
         get_fernet.cache_clear()
 
+    @pytest.fixture(autouse=True)
+    def clear_process_context(self, monkeypatch):
+        """Isolate tests from process-wide execution context left behind by other imports."""
+        monkeypatch.delenv("_AIRFLOW_PROCESS_CONTEXT", raising=False)
+        monkeypatch.delitem(sys.modules, "airflow.sdk.execution_time.task_runner", raising=False)
+
     @pytest.mark.parametrize(
         (
             "uri",
@@ -455,6 +461,28 @@ def test_get_connection_from_secrets_task_sdk_not_found(self, mock_task_sdk_conn
             with pytest.raises(AirflowNotFoundException):
                 Connection.get_connection_from_secrets("test_conn")
 
+    @mock.patch.dict("os.environ", {"_AIRFLOW_PROCESS_CONTEXT": "server"})
+    def test_connection_from_json_uses_core_path_when_server_context(self):
+        """Server context should prefer core Connection.from_json even if comms exist."""
+        fake_task_runner = mock.MagicMock()
+        fake_task_runner.SUPERVISOR_COMMS = True
+
+        with (
+            mock.patch.dict(sys.modules, {"airflow.sdk.execution_time.task_runner": fake_task_runner}),
+            mock.patch(
+                "airflow.sdk.Connection.from_json",
+                side_effect=AssertionError(
+                    "Connection.from_json should not route through Task SDK in server context"
+                ),
+            ),
+        ):
+            result = Connection.from_json('{"conn_type": "http", "host": "localhost"}', conn_id="test_conn")
+
+        assert isinstance(result, Connection)
+        assert result.conn_id == "test_conn"
+        assert result.conn_type == "http"
+        assert result.host == "localhost"
+
     @mock.patch.dict(sys.modules, {"airflow.sdk.execution_time.task_runner": None})
     @mock.patch("airflow.sdk.Connection")
     @mock.patch("airflow.secrets.environment_variables.EnvironmentVariablesBackend.get_connection")
diff --git a/task-sdk/src/airflow/sdk/execution_time/supervisor.py b/task-sdk/src/airflow/sdk/execution_time/supervisor.py
index 76dfd2009ac18..9251bf1c623d1 100644
--- a/task-sdk/src/airflow/sdk/execution_time/supervisor.py
+++ b/task-sdk/src/airflow/sdk/execution_time/supervisor.py
@@ -1922,10 +1922,10 @@ def _send_new_log_fd(self, req_id: int) -> None:
 
 
 @functools.lru_cache(maxsize=1)
-def in_process_api_server():
+def in_process_api_server(*, request_scoped_server_context: bool = False):
     from airflow.api_fastapi.execution_api.app import InProcessExecutionAPI
 
-    api = InProcessExecutionAPI()
+    api = InProcessExecutionAPI(request_scoped_server_context=request_scoped_server_context)
     return api
 
 
@@ -2087,7 +2087,7 @@ def start(  # type: ignore[override]
 
     @staticmethod
     def _api_client(dag=None):
-        api = in_process_api_server()
+        api = in_process_api_server(request_scoped_server_context=True)
         from airflow.api_fastapi.common.dagbag import dag_bag_from_app
 
         if dag is not None:
diff --git a/task-sdk/tests/task_sdk/execution_time/test_supervisor.py b/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
index 8dea3d0793f49..cc8f5e53108e5 100644
--- a/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
+++ b/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
@@ -3439,6 +3439,18 @@ def execute(self, context: Context):
         assert isinstance(result.error, _Failure)
         assert isinstance(collected[0], _Failure)
 
+    def test_api_client_uses_request_scoped_server_context(self):
+        api = mock.Mock()
+        api.transport = httpx.MockTransport(lambda request: httpx.Response(status_code=200, json={}))
+
+        with patch(
+            "airflow.sdk.execution_time.supervisor.in_process_api_server", return_value=api
+        ) as factory:
+            client = InProcessTestSupervisor._api_client()
+
+        factory.assert_called_once_with(request_scoped_server_context=True)
+        client.close()
+
 
 class TestInProcessClient:
     def test_no_retries(self):
@@ -4047,7 +4059,7 @@ def test_api_client_clears_dag_bag_override_when_dag_is_none():
         # First call with a dag sets the override
         mock_dag = MagicMock()
         InProcessTestSupervisor._api_client(dag=mock_dag)
-        api = in_process_api_server()
+        api = in_process_api_server(request_scoped_server_context=True)
         assert dag_bag_from_app in api.app.dependency_overrides
 
         # Second call with dag=None should remove it