diff --git a/changelog.d/10208.bugfix b/changelog.d/10208.bugfix
new file mode 100644
index 0000000000..32b6465717
--- /dev/null
+++ b/changelog.d/10208.bugfix
@@ -0,0 +1 @@
+Fix a bug introduced in v1.35.1 where an `allow` key of a `m.room.join_rules` event could be applied for incorrect room versions and configurations.
diff --git a/synapse/handlers/space_summary.py b/synapse/handlers/space_summary.py
index e953a8afe6..17fc47ce16 100644
--- a/synapse/handlers/space_summary.py
+++ b/synapse/handlers/space_summary.py
@@ -445,14 +445,13 @@ class SpaceSummaryHandler:
             member_event_id = state_ids.get((EventTypes.Member, requester), None)
 
             # If they're in the room they can see info on it.
-            member_event = None
             if member_event_id:
                 member_event = await self._store.get_event(member_event_id)
                 if member_event.membership in (Membership.JOIN, Membership.INVITE):
                     return True
 
             # Otherwise, check if they should be allowed access via membership in a space.
-            if self._event_auth_handler.has_restricted_join_rules(
+            if await self._event_auth_handler.has_restricted_join_rules(
                 state_ids, room_version
             ):
                 allowed_rooms = (
diff --git a/tests/handlers/test_space_summary.py b/tests/handlers/test_space_summary.py
index 2c5e81531b..131d362ccc 100644
--- a/tests/handlers/test_space_summary.py
+++ b/tests/handlers/test_space_summary.py
@@ -11,10 +11,15 @@
 #  WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
 #  See the License for the specific language governing permissions and
 #  limitations under the License.
-from typing import Any, Optional
+from typing import Any, Iterable, Optional, Tuple
 from unittest import mock
 
+from synapse.api.errors import AuthError
 from synapse.handlers.space_summary import _child_events_comparison_key
+from synapse.rest import admin
+from synapse.rest.client.v1 import login, room
+from synapse.server import HomeServer
+from synapse.types import JsonDict
 
 from tests import unittest
 
@@ -79,3 +84,95 @@ class TestSpaceSummarySort(unittest.TestCase):
 
         ev1 = _create_event("!abc:test", "a" * 51)
         self.assertEqual([ev2, ev1], _order(ev1, ev2))
+
+
+class SpaceSummaryTestCase(unittest.HomeserverTestCase):
+    servlets = [
+        admin.register_servlets_for_client_rest_resource,
+        room.register_servlets,
+        login.register_servlets,
+    ]
+
+    def prepare(self, reactor, clock, hs: HomeServer):
+        self.hs = hs
+        self.handler = self.hs.get_space_summary_handler()
+
+        self.user = self.register_user("user", "pass")
+        self.token = self.login("user", "pass")
+
+    def _add_child(self, space_id: str, room_id: str, token: str) -> None:
+        """Add a child room to a space."""
+        self.helper.send_state(
+            space_id,
+            event_type="m.space.child",
+            body={"via": [self.hs.hostname]},
+            tok=token,
+            state_key=room_id,
+        )
+
+    def _assert_rooms(self, result: JsonDict, rooms: Iterable[str]) -> None:
+        """Assert that the expected room IDs are in the response."""
+        self.assertCountEqual([room.get("room_id") for room in result["rooms"]], rooms)
+
+    def _assert_events(
+        self, result: JsonDict, events: Iterable[Tuple[str, str]]
+    ) -> None:
+        """Assert that the expected parent / child room IDs are in the response."""
+        self.assertCountEqual(
+            [
+                (event.get("room_id"), event.get("state_key"))
+                for event in result["events"]
+            ],
+            events,
+        )
+
+    def test_simple_space(self):
+        """Test a simple space with a single room."""
+        space = self.helper.create_room_as(self.user, tok=self.token)
+        room = self.helper.create_room_as(self.user, tok=self.token)
+        self._add_child(space, room, self.token)
+
+        result = self.get_success(self.handler.get_space_summary(self.user, space))
+        # The result should have the space and the room in it, along with a link
+        # from space -> room.
+        self._assert_rooms(result, [space, room])
+        self._assert_events(result, [(space, room)])
+
+    def test_visibility(self):
+        """A user not in a space cannot inspect it."""
+        space = self.helper.create_room_as(self.user, tok=self.token)
+        room = self.helper.create_room_as(self.user, tok=self.token)
+        self._add_child(space, room, self.token)
+
+        user2 = self.register_user("user2", "pass")
+        token2 = self.login("user2", "pass")
+
+        # The user cannot see the space.
+        self.get_failure(self.handler.get_space_summary(user2, space), AuthError)
+
+        # Joining the room causes it to be visible.
+        self.helper.join(space, user2, tok=token2)
+        result = self.get_success(self.handler.get_space_summary(user2, space))
+
+        # The result should only have the space, but includes the link to the room.
+        self._assert_rooms(result, [space])
+        self._assert_events(result, [(space, room)])
+
+    def test_world_readable(self):
+        """A world-readable room is visible to everyone."""
+        space = self.helper.create_room_as(self.user, tok=self.token)
+        room = self.helper.create_room_as(self.user, tok=self.token)
+        self._add_child(space, room, self.token)
+        self.helper.send_state(
+            space,
+            event_type="m.room.history_visibility",
+            body={"history_visibility": "world_readable"},
+            tok=self.token,
+        )
+
+        user2 = self.register_user("user2", "pass")
+
+        # The space should be visible, as well as the link to the room.
+        result = self.get_success(self.handler.get_space_summary(user2, space))
+        self._assert_rooms(result, [space])
+        self._assert_events(result, [(space, room)])