diff --git a/changelog.d/11355.bugfix b/changelog.d/11355.bugfix
new file mode 100644
index 000000000000..91639f14b2ab
--- /dev/null
+++ b/changelog.d/11355.bugfix
@@ -0,0 +1 @@
+Fix a bug introduced in 1.41.0 where space hierarchy responses would be incorrectly reused if multiple users were to make the same request at the same time.
diff --git a/synapse/handlers/room_summary.py b/synapse/handlers/room_summary.py
index fb26ee7ad7bc..8181cc0b5267 100644
--- a/synapse/handlers/room_summary.py
+++ b/synapse/handlers/room_summary.py
@@ -97,7 +97,7 @@ def __init__(self, hs: "HomeServer"):
         # If a user tries to fetch the same page multiple times in quick succession,
         # only process the first attempt and return its result to subsequent requests.
         self._pagination_response_cache: ResponseCache[
-            Tuple[str, bool, Optional[int], Optional[int], Optional[str]]
+            Tuple[str, str, bool, Optional[int], Optional[int], Optional[str]]
         ] = ResponseCache(
             hs.get_clock(),
             "get_room_hierarchy",
@@ -282,7 +282,14 @@ async def get_room_hierarchy(
         # This is due to the pagination process mutating internal state, attempting
         # to process multiple requests for the same page will result in errors.
         return await self._pagination_response_cache.wrap(
-            (requested_room_id, suggested_only, max_depth, limit, from_token),
+            (
+                requester,
+                requested_room_id,
+                suggested_only,
+                max_depth,
+                limit,
+                from_token,
+            ),
             self._get_room_hierarchy,
             requester,
             requested_room_id,
diff --git a/tests/handlers/test_room_summary.py b/tests/handlers/test_room_summary.py
index d3d0bf1ac57e..7b95844b55d3 100644
--- a/tests/handlers/test_room_summary.py
+++ b/tests/handlers/test_room_summary.py
@@ -14,6 +14,8 @@
 from typing import Any, Iterable, List, Optional, Tuple
 from unittest import mock
 
+from twisted.internet.defer import ensureDeferred
+
 from synapse.api.constants import (
     EventContentFields,
     EventTypes,
@@ -316,6 +318,59 @@ def test_visibility(self):
             AuthError,
         )
 
+    def test_room_hierarchy_cache(self) -> None:
+        """In-flight room hierarchy requests are deduplicated."""
+        # Run two `get_room_hierarchy` calls up until they block.
+        deferred1 = ensureDeferred(
+            self.handler.get_room_hierarchy(self.user, self.space)
+        )
+        deferred2 = ensureDeferred(
+            self.handler.get_room_hierarchy(self.user, self.space)
+        )
+
+        # Complete the two calls.
+        result1 = self.get_success(deferred1)
+        result2 = self.get_success(deferred2)
+
+        # Both `get_room_hierarchy` calls should return the same result.
+        expected = [(self.space, [self.room]), (self.room, ())]
+        self._assert_hierarchy(result1, expected)
+        self._assert_hierarchy(result2, expected)
+        self.assertIs(result1, result2)
+
+        # A subsequent `get_room_hierarchy` call should not reuse the result.
+        result3 = self.get_success(
+            self.handler.get_room_hierarchy(self.user, self.space)
+        )
+        self._assert_hierarchy(result3, expected)
+        self.assertIsNot(result1, result3)
+
+    def test_room_hierarchy_cache_sharing(self) -> None:
+        """Room hierarchy responses for different users are not shared."""
+        user2 = self.register_user("user2", "pass")
+
+        # Make the room within the space invite-only.
+        self.helper.send_state(
+            self.room,
+            event_type=EventTypes.JoinRules,
+            body={"join_rule": JoinRules.INVITE},
+            tok=self.token,
+        )
+
+        # Run two `get_room_hierarchy` calls for different users up until they block.
+        deferred1 = ensureDeferred(
+            self.handler.get_room_hierarchy(self.user, self.space)
+        )
+        deferred2 = ensureDeferred(self.handler.get_room_hierarchy(user2, self.space))
+
+        # Complete the two calls.
+        result1 = self.get_success(deferred1)
+        result2 = self.get_success(deferred2)
+
+        # The `get_room_hierarchy` calls should return different results.
+        self._assert_hierarchy(result1, [(self.space, [self.room]), (self.room, ())])
+        self._assert_hierarchy(result2, [(self.space, [self.room])])
+
     def _create_room_with_join_rule(
         self, join_rule: str, room_version: Optional[str] = None, **extra_content
     ) -> str: