diff --git a/distributed/tests/test_worker_state_machine.py b/distributed/tests/test_worker_state_machine.py
index 324d9b4799..94408d1ef8 100644
--- a/distributed/tests/test_worker_state_machine.py
+++ b/distributed/tests/test_worker_state_machine.py
@@ -23,6 +23,7 @@
     ExecuteSuccessEvent,
     Instruction,
     RecommendationsConflict,
+    RefreshWhoHasEvent,
     ReleaseWorkerDataMsg,
     RescheduleEvent,
     RescheduleMsg,
@@ -603,3 +604,46 @@ async def test_missing_to_waiting(c, s, w1, w2, w3):
     await w1.close()
 
     await f1
+
+
+@gen_cluster(client=True, nthreads=[("", 1)] * 3)
+async def test_fetch_to_missing_on_refresh_who_has(c, s, w1, w2, w3):
+    """
+    1. Two tasks, x and y, are only available on a busy worker.
+       The worker sends request-refresh-who-has to the scheduler.
+    2. The scheduler responds that x has become missing, while y has gained an
+       additional replica
+    3. The handler for RefreshWhoHasEvent empties x.who_has and recommends a transition
+       to missing.
+    4. Before the recommendation can be implemented, the same event invokes
+       _ensure_communicating to let y to transition to flight. This in turn pops x from
+       data_needed - but x has an empty who_has, which is an exceptional situation.
+    5. The transition fetch->missing is executed, but x is no longer in
+       data_needed - another exceptional situation.
+    """
+    x = c.submit(inc, 1, key="x", workers=[w1.address])
+    y = c.submit(inc, 2, key="y", workers=[w1.address])
+    await wait([x, y])
+    w1.total_in_connections = 0
+    s.request_acquire_replicas(w3.address, ["x", "y"], stimulus_id="test1")
+
+    # The tasks will now flip-flop between fetch and flight every 150ms
+    # (see Worker.retry_busy_worker_later)
+    await wait_for_state("x", "fetch", w3)
+    await wait_for_state("y", "fetch", w3)
+    assert w1.address in w3.busy_workers
+    # w3 sent {op: request-refresh-who-has, keys: [x, y]}
+    # There also may have been enough time for a refresh-who-has message to come back,
+    # which reiterated what w3 already knew:
+    # {op: refresh-who-has, who_has={x: [w1.address], y: [w1.address]}}
+
+    # Let's instead simulate that, while request-refresh-who-has was in transit,
+    # w2 gained a replica of y and w1 closed down.
+    # When request-refresh-who-has lands, the scheduler will respond:
+    # {op: refresh-who-has, who_has={x: [], y: [w2.address]}}
+    w3.handle_stimulus(
+        RefreshWhoHasEvent(who_has={"x": [], "y": [w2.address]}, stimulus_id="test2")
+    )
+    assert w3.tasks["x"].state == "missing"
+    assert w3.tasks["y"].state == "flight"
+    assert w3.tasks["y"].who_has == {w2.address}
diff --git a/distributed/worker.py b/distributed/worker.py
index d7598ad182..880f741502 100644
--- a/distributed/worker.py
+++ b/distributed/worker.py
@@ -2181,7 +2181,14 @@ def transition_fetch_flight(
     def transition_fetch_missing(
         self, ts: TaskState, *, stimulus_id: str
     ) -> RecsInstrs:
-        self.data_needed.remove(ts)
+        # There's a use case where ts won't be found in self.data_needed, so
+        # `self.data_needed.remove(ts)` would crash:
+        # 1. An event handler empties who_has and pushes a recommendation to missing
+        # 2. The same event handler calls _ensure_communicating, which pops the task
+        #    from data_needed
+        # 3. The recommendation is enacted
+        # See matching code in _ensure_communicating.
+        self.data_needed.discard(ts)
         return self.transition_generic_missing(ts, stimulus_id=stimulus_id)
 
     def transition_memory_released(
@@ -3003,9 +3010,16 @@ def _ensure_communicating(self, *, stimulus_id: str) -> RecsInstrs:
 
             if self.validate:
                 assert ts.state == "fetch"
-                assert ts.who_has
                 assert self.address not in ts.who_has
 
+            if not ts.who_has:
+                # An event handler just emptied who_has and recommended a fetch->missing
+                # transition. Then, the same handler called _ensure_communicating. The
+                # transition hasn't been enacted yet, so the task is still in fetch
+                # state and in data_needed.
+                # See matching code in transition_fetch_missing.
+                continue
+
             workers = [
                 w
                 for w in ts.who_has