diff --git a/.github/workflows/build.yml b/.github/workflows/build.yml
index 873b81fa66f8..3d121564d385 100644
--- a/.github/workflows/build.yml
+++ b/.github/workflows/build.yml
@@ -106,7 +106,45 @@ jobs:
           version: 1.1.308
           working-directory: 'pythonFiles'
 
-  ### Non-smoke tests
+  python-tests:
+    name: Python Tests
+    # The value of runs-on is the OS of the current job (specified in the strategy matrix below) instead of being hardcoded.
+    runs-on: ${{ matrix.os }}
+    defaults:
+      run:
+        working-directory: ${{ env.special-working-directory }}
+    strategy:
+      fail-fast: false
+      matrix:
+        # We're not running CI on macOS for now because it's one less matrix entry to lower the number of runners used,
+        # macOS runners are expensive, and we assume that Ubuntu is enough to cover the Unix case.
+        os: [ubuntu-latest, windows-latest]
+        # Run the tests on the oldest and most recent versions of Python.
+        python: ['3.8', '3.x']
+
+    steps:
+      - name: Checkout
+        uses: actions/checkout@v4
+        with:
+          path: ${{ env.special-working-directory-relative }}
+
+      - name: Use Python ${{ matrix.python }}
+        uses: actions/setup-python@v4
+        with:
+          python-version: ${{ matrix.python }}
+
+      - name: Install base Python requirements
+        uses: brettcannon/pip-secure-install@v1
+        with:
+          requirements-file: '"${{ env.special-working-directory-relative }}/requirements.txt"'
+          options: '-t "${{ env.special-working-directory-relative }}/pythonFiles/lib/python" --no-cache-dir --implementation py'
+
+      - name: Install test requirements
+        run: python -m pip install --upgrade -r build/test-requirements.txt
+
+      - name: Run Python unit tests
+        run: python pythonFiles/tests/run_all.py
+
   tests:
     name: Tests
     if: github.repository == 'microsoft/vscode-python'
@@ -122,7 +160,7 @@ jobs:
         # and we assume that Ubuntu is enough to cover the UNIX case.
         os: [ubuntu-latest, windows-latest]
         python: ['3.x']
-        test-suite: [ts-unit, python-unit, venv, single-workspace, multi-workspace, debugger, functional]
+        test-suite: [ts-unit, venv, single-workspace, multi-workspace, debugger, functional]
     steps:
       - name: Checkout
         uses: actions/checkout@v4
@@ -268,10 +306,6 @@ jobs:
         run: npm run test:unittests
         if: matrix.test-suite == 'ts-unit' && startsWith(matrix.python, '3.')
 
-      - name: Run Python unit tests
-        run: python pythonFiles/tests/run_all.py
-        if: matrix.test-suite == 'python-unit'
-
       # The virtual environment based tests use the `testSingleWorkspace` set of tests
       # with the environment variable `TEST_FILES_SUFFIX` set to `testvirtualenvs`,
       # which is set in the "Prepare environment for venv tests" step.
diff --git a/.github/workflows/pr-check.yml b/.github/workflows/pr-check.yml
index c7335702e991..aa223782de62 100644
--- a/.github/workflows/pr-check.yml
+++ b/.github/workflows/pr-check.yml
@@ -80,7 +80,45 @@ jobs:
           version: 1.1.308
           working-directory: 'pythonFiles'
 
-  ### Non-smoke tests
+  python-tests:
+    name: Python Tests
+    # The value of runs-on is the OS of the current job (specified in the strategy matrix below) instead of being hardcoded.
+    runs-on: ${{ matrix.os }}
+    defaults:
+      run:
+        working-directory: ${{ env.special-working-directory }}
+    strategy:
+      fail-fast: false
+      matrix:
+        # We're not running CI on macOS for now because it's one less matrix entry to lower the number of runners used,
+        # macOS runners are expensive, and we assume that Ubuntu is enough to cover the Unix case.
+        os: [ubuntu-latest, windows-latest]
+        # Run the tests on the oldest and most recent versions of Python.
+        python: ['3.8', '3.x']
+
+    steps:
+      - name: Checkout
+        uses: actions/checkout@v4
+        with:
+          path: ${{ env.special-working-directory-relative }}
+
+      - name: Use Python ${{ matrix.python }}
+        uses: actions/setup-python@v4
+        with:
+          python-version: ${{ matrix.python }}
+
+      - name: Install base Python requirements
+        uses: brettcannon/pip-secure-install@v1
+        with:
+          requirements-file: '"${{ env.special-working-directory-relative }}/requirements.txt"'
+          options: '-t "${{ env.special-working-directory-relative }}/pythonFiles/lib/python" --no-cache-dir --implementation py'
+
+      - name: Install test requirements
+        run: python -m pip install --upgrade -r build/test-requirements.txt
+
+      - name: Run Python unit tests
+        run: python pythonFiles/tests/run_all.py
+
   tests:
     name: Tests
     # The value of runs-on is the OS of the current job (specified in the strategy matrix below) instead of being hardcoded.
@@ -96,7 +134,7 @@ jobs:
         os: [ubuntu-latest, windows-latest]
         # Run the tests on the oldest and most recent versions of Python.
         python: ['3.x']
-        test-suite: [ts-unit, python-unit, venv, single-workspace, debugger, functional]
+        test-suite: [ts-unit, venv, single-workspace, debugger, functional]
 
     steps:
       - name: Checkout
@@ -139,14 +177,12 @@ jobs:
         with:
           requirements-file: '"${{ env.special-working-directory-relative }}/requirements.txt"'
           options: '-t "${{ env.special-working-directory-relative }}/pythonFiles/lib/python" --no-cache-dir --implementation py'
-        if: startsWith(matrix.python, 3.)
 
       - name: Install Jedi requirements
         uses: brettcannon/pip-secure-install@v1
         with:
           requirements-file: '"${{ env.special-working-directory-relative }}/pythonFiles/jedilsp_requirements/requirements.txt"'
           options: '-t "${{ env.special-working-directory-relative }}/pythonFiles/lib/jedilsp" --no-cache-dir --implementation py'
-        if: startsWith(matrix.python, 3.)
 
       - name: Install test requirements
         run: python -m pip install --upgrade -r build/test-requirements.txt
@@ -243,12 +279,6 @@ jobs:
         run: npm run test:unittests
         if: matrix.test-suite == 'ts-unit' && startsWith(matrix.python, 3.)
 
-      # Run the Python tests in our codebase.
-      - name: Run Python unit tests
-        run: |
-          python pythonFiles/tests/run_all.py
-        if: matrix.test-suite == 'python-unit'
-
       # The virtual environment based tests use the `testSingleWorkspace` set of tests
       # with the environment variable `TEST_FILES_SUFFIX` set to `testvirtualenvs`,
       # which is set in the "Prepare environment for venv tests" step.
diff --git a/pythonFiles/unittestadapter/discovery.py b/pythonFiles/unittestadapter/discovery.py
index 6208d24bee9f..69c14cae34e6 100644
--- a/pythonFiles/unittestadapter/discovery.py
+++ b/pythonFiles/unittestadapter/discovery.py
@@ -51,7 +51,7 @@ class PayloadDict(TypedDict):
 class EOTPayloadDict(TypedDict):
     """A dictionary that is used to send a end of transmission post request to the server."""
 
-    command_type: Literal["discovery"] | Literal["execution"]
+    command_type: Union[Literal["discovery"], Literal["execution"]]
     eot: bool
 
 
@@ -113,7 +113,9 @@ def discover_tests(
     return payload
 
 
-def post_response(payload: PayloadDict | EOTPayloadDict, port: int, uuid: str) -> None:
+def post_response(
+    payload: Union[PayloadDict, EOTPayloadDict], port: int, uuid: str
+) -> None:
     # Build the request data (it has to be a POST request or the Node side will not process it), and send it.
     addr = ("localhost", port)
     data = json.dumps(payload)
diff --git a/pythonFiles/unittestadapter/execution.py b/pythonFiles/unittestadapter/execution.py
index 7bbc97e78f31..a208056c6682 100644
--- a/pythonFiles/unittestadapter/execution.py
+++ b/pythonFiles/unittestadapter/execution.py
@@ -172,7 +172,7 @@ class PayloadDict(TypedDict):
 class EOTPayloadDict(TypedDict):
     """A dictionary that is used to send a end of transmission post request to the server."""
 
-    command_type: Literal["discovery"] | Literal["execution"]
+    command_type: Union[Literal["discovery"], Literal["execution"]]
     eot: bool
 
 
@@ -250,7 +250,9 @@ def send_run_data(raw_data, port, uuid):
     post_response(payload, port, uuid)
 
 
-def post_response(payload: PayloadDict | EOTPayloadDict, port: int, uuid: str) -> None:
+def post_response(
+    payload: Union[PayloadDict, EOTPayloadDict], port: int, uuid: str
+) -> None:
     # Build the request data (it has to be a POST request or the Node side will not process it), and send it.
     addr = ("localhost", port)
     global __socket