diff --git a/changelog.d/6873.feature b/changelog.d/6873.feature
new file mode 100644
index 0000000000..bbedf8f7f0
--- /dev/null
+++ b/changelog.d/6873.feature
@@ -0,0 +1 @@
+Add ability to route federation user device queries to workers.
diff --git a/docs/workers.md b/docs/workers.md
index 82442d6a0a..6f7ec58780 100644
--- a/docs/workers.md
+++ b/docs/workers.md
@@ -176,6 +176,7 @@ endpoints matching the following regular expressions:
     ^/_matrix/federation/v1/query_auth/
     ^/_matrix/federation/v1/event_auth/
     ^/_matrix/federation/v1/exchange_third_party_invite/
+    ^/_matrix/federation/v1/user/devices/
     ^/_matrix/federation/v1/send/
     ^/_matrix/federation/v1/get_groups_publicised$
     ^/_matrix/key/v2/query
diff --git a/synapse/app/federation_reader.py b/synapse/app/federation_reader.py
index 5e17ef1396..d055d11b23 100644
--- a/synapse/app/federation_reader.py
+++ b/synapse/app/federation_reader.py
@@ -33,6 +33,7 @@ from synapse.metrics import METRICS_PREFIX, MetricsResource, RegistryProxy
 from synapse.replication.slave.storage._base import BaseSlavedStore
 from synapse.replication.slave.storage.account_data import SlavedAccountDataStore
 from synapse.replication.slave.storage.appservice import SlavedApplicationServiceStore
+from synapse.replication.slave.storage.devices import SlavedDeviceStore
 from synapse.replication.slave.storage.directory import DirectoryStore
 from synapse.replication.slave.storage.events import SlavedEventStore
 from synapse.replication.slave.storage.groups import SlavedGroupServerStore
@@ -68,6 +69,7 @@ class FederationReaderSlavedStore(
     SlavedKeyStore,
     SlavedRegistrationStore,
     SlavedGroupServerStore,
+    SlavedDeviceStore,
     RoomStore,
     DirectoryStore,
     SlavedTransactionStore,
diff --git a/synapse/federation/federation_server.py b/synapse/federation/federation_server.py
index a6c966a393..7f9da49326 100644
--- a/synapse/federation/federation_server.py
+++ b/synapse/federation/federation_server.py
@@ -81,6 +81,8 @@ class FederationServer(FederationBase):
         self.handler = hs.get_handlers().federation_handler
         self.state = hs.get_state_handler()
 
+        self.device_handler = hs.get_device_handler()
+
         self._server_linearizer = Linearizer("fed_server")
         self._transaction_linearizer = Linearizer("fed_txn_handler")
 
@@ -523,8 +525,9 @@ class FederationServer(FederationBase):
     def on_query_client_keys(self, origin, content):
         return self.on_query_request("client_keys", content)
 
-    def on_query_user_devices(self, origin, user_id):
-        return self.on_query_request("user_devices", user_id)
+    async def on_query_user_devices(self, origin: str, user_id: str):
+        keys = await self.device_handler.on_federation_query_user_devices(user_id)
+        return 200, keys
 
     @trace
     async def on_claim_client_keys(self, origin, content):
diff --git a/synapse/handlers/device.py b/synapse/handlers/device.py
index a9bd431486..6d8e48ed39 100644
--- a/synapse/handlers/device.py
+++ b/synapse/handlers/device.py
@@ -225,6 +225,22 @@ class DeviceWorkerHandler(BaseHandler):
 
         return result
 
+    @defer.inlineCallbacks
+    def on_federation_query_user_devices(self, user_id):
+        stream_id, devices = yield self.store.get_devices_with_keys_by_user(user_id)
+        master_key = yield self.store.get_e2e_cross_signing_key(user_id, "master")
+        self_signing_key = yield self.store.get_e2e_cross_signing_key(
+            user_id, "self_signing"
+        )
+
+        return {
+            "user_id": user_id,
+            "stream_id": stream_id,
+            "devices": devices,
+            "master_key": master_key,
+            "self_signing_key": self_signing_key,
+        }
+
 
 class DeviceHandler(DeviceWorkerHandler):
     def __init__(self, hs):
@@ -239,9 +255,6 @@ class DeviceHandler(DeviceWorkerHandler):
         federation_registry.register_edu_handler(
             "m.device_list_update", self.device_list_updater.incoming_device_list_update
         )
-        federation_registry.register_query_handler(
-            "user_devices", self.on_federation_query_user_devices
-        )
 
         hs.get_distributor().observe("user_left_room", self.user_left_room)
 
@@ -456,22 +469,6 @@ class DeviceHandler(DeviceWorkerHandler):
 
         self.notifier.on_new_event("device_list_key", position, users=[from_user_id])
 
-    @defer.inlineCallbacks
-    def on_federation_query_user_devices(self, user_id):
-        stream_id, devices = yield self.store.get_devices_with_keys_by_user(user_id)
-        master_key = yield self.store.get_e2e_cross_signing_key(user_id, "master")
-        self_signing_key = yield self.store.get_e2e_cross_signing_key(
-            user_id, "self_signing"
-        )
-
-        return {
-            "user_id": user_id,
-            "stream_id": stream_id,
-            "devices": devices,
-            "master_key": master_key,
-            "self_signing_key": self_signing_key,
-        }
-
     @defer.inlineCallbacks
     def user_left_room(self, user, room_id):
         user_id = user.to_string()