diff --git a/supervisor/api/proxy.py b/supervisor/api/proxy.py
index 01078625d..2d7ff49c8 100644
--- a/supervisor/api/proxy.py
+++ b/supervisor/api/proxy.py
@@ -222,6 +222,11 @@ class APIProxy(CoreSysAttributes):
             raise HTTPBadGateway()
         _LOGGER.info("Home Assistant WebSocket API request initialize")
 
+        # Check if transport is still valid before WebSocket upgrade
+        if request.transport is None:
+            _LOGGER.warning("WebSocket connection lost before upgrade")
+            raise web.HTTPBadRequest(reason="Connection closed")
+
         # init server
         server = web.WebSocketResponse(heartbeat=30)
         await server.prepare(request)
diff --git a/tests/api/test_proxy.py b/tests/api/test_proxy.py
index 9694e4f3f..c598d50cf 100644
--- a/tests/api/test_proxy.py
+++ b/tests/api/test_proxy.py
@@ -223,6 +223,34 @@ async def test_proxy_auth_abort_log(
         )
 
 
+async def test_websocket_transport_none(
+    coresys,
+    caplog: pytest.LogCaptureFixture,
+):
+    """Test WebSocket connection with transport None is handled gracefully."""
+    from aiohttp import web
+
+    # Get the API proxy instance from coresys
+    api_proxy = APIProxy.__new__(APIProxy)
+    api_proxy.coresys = coresys
+
+    # Create a mock request with transport set to None to simulate connection loss
+    mock_request = AsyncMock(spec=web.Request)
+    mock_request.transport = None
+
+    caplog.clear()
+    with caplog.at_level(logging.WARNING):
+        # This should raise HTTPBadRequest, not AssertionError
+        with pytest.raises(web.HTTPBadRequest) as exc_info:
+            await api_proxy.websocket(mock_request)
+
+        # Verify the error reason
+        assert exc_info.value.reason == "Connection closed"
+
+        # Verify the warning was logged
+        assert "WebSocket connection lost before upgrade" in caplog.text
+
+
 @pytest.mark.parametrize("path", ["", "mock_path"])
 async def test_api_proxy_get_request(
     api_client: TestClient,