diff --git a/changelog.d/19460.bugfix b/changelog.d/19460.bugfix
new file mode 100644
index 0000000000..fe44c2ddf6
--- /dev/null
+++ b/changelog.d/19460.bugfix
@@ -0,0 +1 @@
+Fix `/sync` missing membership event in `state_after` (experimental [MSC4222](https://github.com/matrix-org/matrix-spec-proposals/pull/4222) implementation) in some scenarios.
diff --git a/docker/complement/conf/workers-shared-extra.yaml.j2 b/docker/complement/conf/workers-shared-extra.yaml.j2
index 120b3b9496..9fd7fc954a 100644
--- a/docker/complement/conf/workers-shared-extra.yaml.j2
+++ b/docker/complement/conf/workers-shared-extra.yaml.j2
@@ -141,6 +141,8 @@ experimental_features:
   msc4306_enabled: true
   # Sticky Events
   msc4354_enabled: true
+  # `/sync` `state_after`
+  msc4222_enabled: true
 
 server_notices:
   system_mxid_localpart: _server
diff --git a/scripts-dev/complement.sh b/scripts-dev/complement.sh
index 9a18a621ee..fec005fdb1 100755
--- a/scripts-dev/complement.sh
+++ b/scripts-dev/complement.sh
@@ -264,6 +264,7 @@ main() {
     ./tests/msc4140
     ./tests/msc4155
     ./tests/msc4306
+    ./tests/msc4222
   )
 
   # Export the list of test packages as a space-separated environment variable, so other
diff --git a/synapse/handlers/sync.py b/synapse/handlers/sync.py
index 2f405004de..a32748c2a9 100644
--- a/synapse/handlers/sync.py
+++ b/synapse/handlers/sync.py
@@ -1046,9 +1046,18 @@ class SyncHandler:
                     if event.sender not in first_event_by_sender_map:
                         first_event_by_sender_map[event.sender] = event
 
-                    # We need the event's sender, unless their membership was in a
-                    # previous timeline event.
-                    if (EventTypes.Member, event.sender) not in timeline_state:
+                    # When using `state_after`, there is no special treatment with
+                    # regards to state also being in the `timeline`. Always fetch
+                    # relevant membership regardless of whether the state event is in
+                    # the `timeline`.
+                    if sync_config.use_state_after:
+                        members_to_fetch.add(event.sender)
+                    # For `state`, the client is supposed to do a flawed re-construction
+                    # of state over time by starting with the given `state` and layering
+                    # on state from the `timeline` as you go (flawed because state
+                    # resolution). In this case, we only need their membership in
+                    # `state` when their membership isn't already in the `timeline`.
+                    elif (EventTypes.Member, event.sender) not in timeline_state:
                         members_to_fetch.add(event.sender)
                     # FIXME: we also care about invite targets etc.