diff --git a/.github/workflows/enterprise-integration-tests.yml b/.github/workflows/enterprise-integration-tests.yml
new file mode 100644
index 000000000000..e0e1610adf98
--- /dev/null
+++ b/.github/workflows/enterprise-integration-tests.yml
@@ -0,0 +1,42 @@
+name: Run Enterprise Integration Tests
+
+on:
+  push:
+    branches:
+      - main
+  pull_request:
+
+concurrency:
+  group: ${{ github.workflow }}-${{ (github.head_ref && github.ref) || github.run_id }}
+  cancel-in-progress: true
+
+jobs:
+  test-enterprise-integration:
+    name: Enterprise Python Integration Tests
+    runs-on: ubuntu-24.04
+    strategy:
+      matrix:
+        python-version: ["3.12"]
+    steps:
+      - uses: actions/checkout@v6
+      - name: Install poetry via pipx
+        run: pipx install poetry
+      - name: Set up Python
+        uses: actions/setup-python@v5
+        with:
+          python-version: ${{ matrix.python-version }}
+          cache: "poetry"
+      - name: Install Python dependencies using Poetry
+        working-directory: ./enterprise
+        run: poetry install --with dev,test
+      - name: Run Integration Tests
+        # Use base working directory for coverage paths to line up.
+        run: PYTHONPATH=".:$PYTHONPATH" poetry run --project=enterprise pytest --forked -n auto -s -p no:ddtrace -p no:ddtrace.pytest_bdd -p no:ddtrace.pytest_benchmark ./enterprise/tests/integration --cov=enterprise --cov-branch
+        env:
+          COVERAGE_FILE: ".coverage.enterprise.integration.${{ matrix.python-version }}"
+      - name: Store coverage file
+        uses: actions/upload-artifact@v7
+        with:
+          name: coverage-enterprise-integration
+          path: ".coverage.enterprise.integration.${{ matrix.python-version }}"
+          include-hidden-files: true
diff --git a/enterprise/pyproject.toml b/enterprise/pyproject.toml
index b029d2178f11..c94b65397cde 100644
--- a/enterprise/pyproject.toml
+++ b/enterprise/pyproject.toml
@@ -92,6 +92,9 @@ lint.pydocstyle.convention = "google"
 [tool.pytest.ini_options]
 asyncio_mode = "auto"
 asyncio_default_fixture_loop_scope = "function"
+markers = [
+  "integration: mark test as requiring a real database (deselect with '-m not integration')",
+]
 
 [tool.coverage.run]
 relative_files = true
diff --git a/enterprise/tests/integration/__init__.py b/enterprise/tests/integration/__init__.py
new file mode 100644
index 000000000000..e69de29bb2d1
diff --git a/enterprise/tests/integration/conftest.py b/enterprise/tests/integration/conftest.py
new file mode 100644
index 000000000000..ec6bf107e36b
--- /dev/null
+++ b/enterprise/tests/integration/conftest.py
@@ -0,0 +1,99 @@
+import os
+
+import pytest
+from sqlalchemy import create_engine
+from sqlalchemy.ext.asyncio import AsyncSession, async_sessionmaker, create_async_engine
+from sqlalchemy.orm import sessionmaker
+
+# Import all models so their tables are created.
+from storage.api_key import ApiKey  # noqa: F401
+from storage.base import Base
+from storage.billing_session import BillingSession  # noqa: F401
+from storage.conversation_work import ConversationWork  # noqa: F401
+from storage.device_code import DeviceCode  # noqa: F401
+from storage.feedback import Feedback  # noqa: F401
+from storage.github_app_installation import GithubAppInstallation  # noqa: F401
+from storage.org import Org  # noqa: F401
+from storage.org_git_claim import OrgGitClaim  # noqa: F401
+from storage.org_invitation import OrgInvitation  # noqa: F401
+from storage.org_member import OrgMember  # noqa: F401
+from storage.role import Role  # noqa: F401
+from storage.slack_conversation import SlackConversation  # noqa: F401
+from storage.stored_conversation_metadata import (
+    StoredConversationMetadata,  # noqa: F401
+)
+from storage.stored_conversation_metadata_saas import (  # noqa: F401
+    StoredConversationMetadataSaas,
+)
+from storage.stored_offline_token import StoredOfflineToken  # noqa: F401
+from storage.stripe_customer import StripeCustomer  # noqa: F401
+from storage.user import User  # noqa: F401
+from storage.user_settings import UserSettings  # noqa: F401
+
+
+def pytest_collection_modifyitems(config, items):
+    for item in items:
+        item.add_marker(pytest.mark.integration)
+
+
+@pytest.fixture(autouse=True)
+def allow_short_context_windows():
+    old = os.environ.get('ALLOW_SHORT_CONTEXT_WINDOWS')
+    os.environ['ALLOW_SHORT_CONTEXT_WINDOWS'] = 'true'
+    try:
+        yield
+    finally:
+        if old is None:
+            os.environ.pop('ALLOW_SHORT_CONTEXT_WINDOWS', None)
+        else:
+            os.environ['ALLOW_SHORT_CONTEXT_WINDOWS'] = old
+
+
+@pytest.fixture(scope='function')
+def db_path(tmp_path):
+    """Create a unique temp file path for each test."""
+    return str(tmp_path / 'test.db')
+
+
+@pytest.fixture
+def engine(db_path):
+    """Create a sync engine with tables using file-based DB."""
+    engine = create_engine(
+        f'sqlite:///{db_path}', connect_args={'check_same_thread': False}
+    )
+    Base.metadata.create_all(engine)
+    try:
+        yield engine
+    finally:
+        engine.dispose()
+
+
+@pytest.fixture
+def session_maker(engine):
+    return sessionmaker(bind=engine)
+
+
+@pytest.fixture
+def async_engine(engine, db_path):
+    """Create an async engine using the SAME file-based database.
+
+    Depends on engine so tables are already created before async tests run.
+    """
+    ae = create_async_engine(
+        f'sqlite+aiosqlite:///{db_path}',
+        connect_args={'check_same_thread': False},
+    )
+    try:
+        yield ae
+    finally:
+        ae.dispose()
+
+
+@pytest.fixture
+async def async_session_maker(async_engine):
+    """Create an async session maker bound to the async engine."""
+    return async_sessionmaker(
+        bind=async_engine,
+        class_=AsyncSession,
+        expire_on_commit=False,
+    )
diff --git a/enterprise/tests/unit/test_api_key_store.py b/enterprise/tests/integration/test_api_key_store.py
similarity index 100%
rename from enterprise/tests/unit/test_api_key_store.py
rename to enterprise/tests/integration/test_api_key_store.py
diff --git a/enterprise/tests/unit/storage/test_api_key_store.py b/enterprise/tests/integration/test_api_key_store_system_keys.py
similarity index 100%
rename from enterprise/tests/unit/storage/test_api_key_store.py
rename to enterprise/tests/integration/test_api_key_store_system_keys.py
diff --git a/enterprise/tests/unit/test_org_store.py b/enterprise/tests/integration/test_org_store.py
similarity index 100%
rename from enterprise/tests/unit/test_org_store.py
rename to enterprise/tests/integration/test_org_store.py