diff --git a/src/apify/storage_clients/_apify/_request_queue_shared_client.py b/src/apify/storage_clients/_apify/_request_queue_shared_client.py
index 4a00e8bc..278b79f2 100644
--- a/src/apify/storage_clients/_apify/_request_queue_shared_client.py
+++ b/src/apify/storage_clients/_apify/_request_queue_shared_client.py
@@ -235,8 +235,8 @@ async def mark_request_as_handled(self, request: Request) -> ProcessedRequest |
                 processed_request=processed_request,
                 hydrated_request=request,
             )
-        except Exception as exc:
-            logger.debug(f'Error marking request {request.unique_key} as handled: {exc!s}')
+        except Exception:
+            logger.exception(f'Error marking request {request.unique_key} as handled.')
             return None
         else:
             return processed_request
diff --git a/src/apify/storage_clients/_apify/_request_queue_single_client.py b/src/apify/storage_clients/_apify/_request_queue_single_client.py
index 7cc202bb..e1a4fa41 100644
--- a/src/apify/storage_clients/_apify/_request_queue_single_client.py
+++ b/src/apify/storage_clients/_apify/_request_queue_single_client.py
@@ -201,27 +201,27 @@ async def mark_request_as_handled(self, request: Request) -> ProcessedRequest |
         # Set the handled_at timestamp if not already set
         request_id = unique_key_to_request_id(request.unique_key)
 
+        if cached_request := self._requests_cache.get(request_id):
+            cached_request.handled_at = request.handled_at
+
         if request.handled_at is None:
             request.handled_at = datetime.now(tz=timezone.utc)
             self.metadata.handled_request_count += 1
             self.metadata.pending_request_count -= 1
 
-        if cached_request := self._requests_cache.get(request_id):
-            cached_request.handled_at = request.handled_at
-
         try:
+            # Remember that we handled this request, to optimize local deduplication.
+            self._requests_already_handled.add(request_id)
+            self._requests_in_progress.discard(request_id)
+            # Remove request from cache, it will most likely not be needed.
+            self._requests_cache.pop(request_id, None)
             # Update the request in the API
             # Works as upsert - adds the request if it does not exist yet. (Local request that was handled before
             # adding to the queue.)
             processed_request = await self._update_request(request)
-            # Remember that we handled this request, to optimize local deduplication.
-            self._requests_already_handled.add(request_id)
-            # Remove request from cache. It will most likely not be needed.
-            self._requests_cache.pop(request_id)
-            self._requests_in_progress.discard(request_id)
 
-        except Exception as exc:
-            logger.debug(f'Error marking request {request.unique_key} as handled: {exc!s}')
+        except Exception:
+            logger.exception(f'Error marking request {request.unique_key} as handled.')
             return None
         else:
             return processed_request
@@ -303,6 +303,11 @@ async def _list_head(self) -> None:
                 # Ignore requests that are already in progress, we will not process them again.
                 continue
 
+            if request_id in self._requests_already_handled:
+                # Request is locally known to be handled, but platform is not aware of it.
+                # This can be either due to delay in API data propagation or failed API call to mark it as handled.
+                continue
+
             if request.was_already_handled:
                 # Do not cache fully handled requests, we do not need them. Just cache their id.
                 self._requests_already_handled.add(request_id)
diff --git a/tests/integration/apify_api/test_request_queue.py b/tests/integration/apify_api/test_request_queue.py
index e90c1600..9c8c7f96 100644
--- a/tests/integration/apify_api/test_request_queue.py
+++ b/tests/integration/apify_api/test_request_queue.py
@@ -1192,3 +1192,40 @@ def return_unprocessed_requests(requests: list[dict], *_: Any, **__: Any) -> dic
     Actor.log.info(stats_after)
 
     assert (stats_after['writeCount'] - stats_before['writeCount']) == 1
+
+
+async def test_request_queue_api_fail_when_marking_as_handled(
+    apify_token: str, monkeypatch: pytest.MonkeyPatch
+) -> None:
+    """Test that single-access based Apify RQ can deal with API failures when marking requests as handled.
+
+    Single-access based Apify RQ is aware that local information is reliable, so even if marking as handled fails
+    during API call, the RQ correctly tracks the handling information locally. It can even fix the missing handled
+    information on the platform later, when fetching next request later.
+    """
+
+    monkeypatch.setenv(ApifyEnvVars.TOKEN, apify_token)
+    async with Actor:
+        rq = await RequestQueue.open(storage_client=ApifyStorageClient(request_queue_access='single'))
+
+        try:
+            request = Request.from_url('http://example.com')
+            # Fetch request
+            await rq.add_request(request)
+            assert request == await rq.fetch_next_request()
+
+            # Mark as handled, but simulate API failure.
+            with mock.patch.object(
+                rq._client._api_client, 'update_request', side_effect=Exception('Simulated API failure')
+            ):
+                await rq.mark_request_as_handled(request)
+            assert not (await rq.get_request(request.unique_key)).was_already_handled
+
+            # RQ with `request_queue_access="single"` knows, that the local information is reliable, so it knows it
+            # handled this request already despite the platform not being aware of it.
+            assert not await rq.fetch_next_request()
+            assert await rq.is_finished()
+            assert await rq.is_empty()
+
+        finally:
+            await rq.drop()