diff --git a/.github/workflows/testing.yml b/.github/workflows/testing.yml
index 12b3bd6a56..1a48a305ed 100644
--- a/.github/workflows/testing.yml
+++ b/.github/workflows/testing.yml
@@ -974,6 +974,7 @@ jobs:
   build-windows:
     name: Build on Windows
     runs-on: windows-latest
+    needs: build
     timeout-minutes: 30
 
     steps:
@@ -1012,6 +1013,15 @@ jobs:
           npm ci
           npm run build
 
+      - name: Download built component folders
+        uses: actions/download-artifact@v4
+        with:
+          name: dash-components
+          path: ${{ github.workspace }}/dash
+
+      - name: Run Windows-specific unit tests
+        run: python -m pytest tests/unit/test_resources.py
+
   dcc-lint:
     name: DCC Lint Tests (Python ${{ matrix.python-version }})
     needs: [build, changes_filter]
diff --git a/CHANGELOG.md b/CHANGELOG.md
index f31991146e..d7d555d30b 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -38,6 +38,7 @@ This project adheres to [Semantic Versioning](https://semver.org/).
 - [#3881](https://github.com/plotly/dash/pull/3881) Fix components rendered as props (eg. `dcc.Dropdown` option labels, `dcc.Tab` labels) crashing or failing to update when the host subtree was replaced by a callback; out-of-tree `ExternalWrapper` components now re-insert themselves and update in place.
 - [#3929](https://github.com/plotly/dash/issues/3929) Fix components that set their own initial state on mount (eg. `dash-bootstrap-components` `Tabs`) not applying it on first render, because descendant layout hashes were reset on the first fresh render (regression introduced in 4.2.0 by [#3570](https://github.com/plotly/dash/pull/3570)).
 - [#3948](https://github.com/plotly/dash/issues/3948) Fix page getting progressively slower as callbacks append children
+- [#3002](https://github.com/plotly/dash/issues/3002) Fix page loads failing with a 500 error on Windows when Dash is imported from an extended-length (`\\?\`) path, as in JupyterLab Desktop. Package resource paths are now joined with the OS separator instead of `/`.
 
 ## [4.4.1] - 2026-07-21
 
diff --git a/dash/dash.py b/dash/dash.py
index ed1ed5ebc8..cb0d849938 100644
--- a/dash/dash.py
+++ b/dash/dash.py
@@ -1261,7 +1261,7 @@ def _get_worker_url(
         # Build fingerprinted URL (same pattern as _collect_and_register_resources)
         module_path = os.path.join(
             os.path.dirname(sys.modules[namespace].__file__),  # type: ignore
-            relative_path,
+            *relative_path.split("/"),
         )
 
         # Use a fallback if the file doesn't exist yet (during development)
@@ -1302,9 +1302,11 @@ def _relative_url_path(relative_package_path="", namespace=""):
             else:
                 version = importlib.import_module(namespace).__version__
 
+            # Split on "/" so the file path uses the OS separator: Windows
+            # extended-length paths (\\?\ prefix) reject forward slashes.
             module_path = os.path.join(  # type: ignore[reportCallIssue]
                 os.path.dirname(sys.modules[namespace].__file__),  # type: ignore[reportCallIssue]
-                relative_package_path,
+                *relative_package_path.split("/"),
             )
 
             modified = int(os.stat(module_path).st_mtime)
@@ -1489,7 +1491,7 @@ def index(self, *_args, **_kwargs):
 
         if self._favicon:
             favicon_mod_time = os.path.getmtime(
-                os.path.join(self.config.assets_folder, self._favicon)
+                os.path.join(self.config.assets_folder, *self._favicon.split("/"))
             )
             favicon_url = f"{self.get_asset_url(self._favicon)}?m={favicon_mod_time}"
         else:
diff --git a/tests/unit/test_resources.py b/tests/unit/test_resources.py
index 413514de18..cbbf52964b 100644
--- a/tests/unit/test_resources.py
+++ b/tests/unit/test_resources.py
@@ -1,4 +1,8 @@
+import os
+import sys
+
 import mock
+import pytest
 import dash
 from dash import dcc, html  # noqa: F401
 
@@ -253,3 +257,28 @@ def test_multiple_external_urls_with_attributes():
         {"src": "https://example.com/script1.js", "type": "module"},
         {"src": "https://example.com/script2.js", "type": "module"},
     ]
+
+
+@pytest.mark.skipif(
+    sys.platform != "win32", reason="extended-length paths only exist on Windows"
+)
+def test_index_with_windows_extended_length_paths(tmp_path, monkeypatch):
+    """Dash and the assets folder under extended-length paths (JupyterLab Desktop).
+
+    Windows uses these paths verbatim, so a "/" inside one is an invalid name.
+    """
+    monkeypatch.setattr(dash, "__file__", "\\\\?\\" + os.path.abspath(dash.__file__))
+    icons = tmp_path / "assets" / "icons"
+    icons.mkdir(parents=True)
+    (icons / "favicon.ico").write_bytes(b"")
+
+    app = dash.Dash(__name__, assets_folder="\\\\?\\" + str(tmp_path / "assets"))
+    app.layout = html.Div()
+
+    response = app.server.test_client().get("/")
+
+    assert response.status_code == 200
+    body = response.get_data(as_text=True)
+    assert "/_dash-component-suites/dash/deps/polyfill@" in body
+    assert "dash-stream-worker.v" in body
+    assert "/assets/icons/favicon.ico?m=" in body