diff --git a/datalab/tests/conftest.py b/datalab/tests/conftest.py
index baf39f9aa..b2a5ade19 100644
--- a/datalab/tests/conftest.py
+++ b/datalab/tests/conftest.py
@@ -8,6 +8,7 @@
 executed before running any tests.
 """
 
+import gc
 import os
 import os.path as osp
 
@@ -23,6 +24,7 @@
 import skimage
 from guidata.config import ValidationMode, set_validation_mode
 from guidata.utils.gitreport import format_git_info_for_pytest, get_git_info_for_modules
+from qtpy import QtCore as QC
 from sigima.tests import helpers
 
 import datalab
@@ -143,3 +145,11 @@ def reset_cwd(request):  # pylint: disable=unused-argument
 def pytest_runtest_teardown(item, nextitem):  # pylint: disable=unused-argument
     """Run teardown after each test."""
     PluginRegistry.unregister_all_plugins()
+    # Destroy the widgets of the test now, rather than during a later test: closed
+    # widgets deleted later (e.g. the internal console) are only deleted by the
+    # next event loop, and main windows are part of reference cycles, only
+    # destroyed when the garbage collector runs, possibly amid Qt operations
+    if QC.QCoreApplication.instance() is not None:
+        QC.QCoreApplication.processEvents()
+        QC.QCoreApplication.sendPostedEvents(None, QC.QEvent.DeferredDelete)
+    gc.collect()
diff --git a/datalab/webapi/actions.py b/datalab/webapi/actions.py
index ebd44266f..a23e733ab 100644
--- a/datalab/webapi/actions.py
+++ b/datalab/webapi/actions.py
@@ -279,9 +279,21 @@ def _on_server_error(self, message: str) -> None:
         self._on_server_stopped()
 
     def cleanup(self) -> None:
-        """Clean up resources on shutdown."""
-        if self._controller is not None and self._controller.is_running:
-            self._controller.stop()
+        """Clean up resources on shutdown.
+
+        The Web API controller is shared by all main windows: once this one is
+        closed, the controller must neither keep it alive nor notify its actions.
+        """
+        controller = self._controller
+        if controller is None:
+            return
+        if controller.is_running:
+            controller.stop()
+        controller.server_started.disconnect(self._on_server_started)
+        controller.server_stopped.disconnect(self._on_server_stopped)
+        controller.server_error.disconnect(self._on_server_error)
+        controller.release_main_window(self._main_window)
+        self._controller = None
 
     def show_connection_info(self) -> None:
         """Show connection info dialog or copy to clipboard.
diff --git a/datalab/webapi/controller.py b/datalab/webapi/controller.py
index bdc8c59ae..50d2fe5b9 100644
--- a/datalab/webapi/controller.py
+++ b/datalab/webapi/controller.py
@@ -106,6 +106,18 @@ def set_main_window(self, main_window: DLMainWindow) -> None:
         """
         self._main_window = main_window
 
+    def release_main_window(self, main_window: DLMainWindow) -> None:
+        """Release the main window reference, if it is the given one.
+
+        The controller being shared by all main windows, a closed main window
+        must not be kept alive by its reference.
+
+        Args:
+            main_window: The DataLab main window being closed.
+        """
+        if self._main_window is main_window:
+            self._main_window = None
+
     @property
     def is_running(self) -> bool:
         """Check if the server is running."""
@@ -337,6 +349,11 @@ def stop(self) -> None:
 
         self._uvicorn_server = None
         self._adapter = None
+        # pylint: disable=import-outside-toplevel
+        from datalab.webapi.routes import set_adapter
+
+        # The adapter references the main window
+        set_adapter(None)
         self._url = None
         self._token = None
 
diff --git a/datalab/webapi/routes.py b/datalab/webapi/routes.py
index 74f54f27d..f6624e1bb 100644
--- a/datalab/webapi/routes.py
+++ b/datalab/webapi/routes.py
@@ -60,8 +60,8 @@
 _LOCALHOST_NO_TOKEN: bool = False
 
 
-def set_adapter(adapter: WorkspaceAdapter) -> None:
-    """Set the workspace adapter for route handlers."""
+def set_adapter(adapter: WorkspaceAdapter | None) -> None:
+    """Set the workspace adapter for route handlers (None when stopped)."""
     global _ADAPTER  # noqa: PLW0603  # pylint: disable=global-statement
     _ADAPTER = adapter