diff --git a/packages/reflex-components-core/src/reflex_components_core/core/_upload.py b/packages/reflex-components-core/src/reflex_components_core/core/_upload.py
index 423bc83403c..11be8771a9a 100644
--- a/packages/reflex-components-core/src/reflex_components_core/core/_upload.py
+++ b/packages/reflex-components-core/src/reflex_components_core/core/_upload.py
@@ -796,7 +796,8 @@ async def upload_file(request: Request):
         Raises:
             UploadValueError: If the handler does not have a supported annotation.
             UploadTypeError: If a non-streaming upload is wired to a background task.
-            HTTPException: when the request does not include token / handler headers.
+            HTTPException: when the request does not include token / handler headers,
+                or when the handler header does not name a registered event handler.
         """
         from reflex_base.event import (
             resolve_upload_chunk_handler_param,
@@ -805,9 +806,14 @@ async def upload_file(request: Request):
         from reflex_base.registry import RegistrationContext
 
         token, handler_name = _require_upload_headers(request)
-        registered_event_handler = RegistrationContext.get().event_handlers[
+        registered_event_handler = RegistrationContext.get().event_handlers.get([
             handler_name
-        ]
+        ])
+        if registered_event_handler is None:
+            raise HTTPException(
+                status_code=400,
+                detail=f"Unknown upload event handler: {handler_name!r}.",
+            )
         event_handler = registered_event_handler.handler
 
         if event_handler.is_background:
diff --git a/tests/units/test_app.py b/tests/units/test_app.py
index c50af0271db..2d9953a0f94 100644
--- a/tests/units/test_app.py
+++ b/tests/units/test_app.py
@@ -36,6 +36,7 @@
 from reflex_components_radix.themes.typography.text import Text
 from starlette.applications import Starlette
 from starlette.datastructures import FormData, Headers, UploadFile
+from starlette.exceptions import HTTPException
 from starlette.requests import ClientDisconnect
 from starlette.responses import StreamingResponse
 from starlette_admin.auth import AuthProvider
@@ -1434,6 +1435,37 @@ async def form():  # noqa: RUF029
 
     await app.state_manager.close()
 
+@pytest.mark.asyncio
+async def test_upload_file_unknown_handler_returns_400(
+    token: str,
+):
+    """Test that an unregistered upload event handler raises a controlled 400.
+
+    A stale, misspelled, or since-removed handler name in the
+    ``reflex-event-handler`` header must not fall through to an unhandled
+    ``KeyError`` (which Starlette would surface as a 500); it should raise a
+    ``HTTPException`` before any form parsing or event dispatch happens.
+
+    Args:
+        token: a Token.
+    """
+    app = App(_state=State)
+
+    request_mock = unittest.mock.Mock()
+    request_mock.headers = {
+        "reflex-client-token": token,
+        "reflex-event-handler": "no.such.State.handler",
+    }
+
+    fn = upload(app)
+    with pytest.raises(HTTPException) as err:
+        await fn(request_mock)
+    assert err.value.status_code == 400
+    assert err.value.detail == "Unknown upload event handler: 'no.such.State.handler'."
+    # The form should never have been read: the handler lookup fails first.
+    request_mock.form.assert_not_called()
+    await app.state_manager.close()
+
 
 @pytest.mark.asyncio
 @pytest.mark.parametrize(