diff --git a/changelog.d/6899.bugfix b/changelog.d/6899.bugfix
new file mode 100644
index 000000000..efa8a40b1
--- /dev/null
+++ b/changelog.d/6899.bugfix
@@ -0,0 +1 @@
+Improve error responses when accessing remote public room lists.
\ No newline at end of file
diff --git a/synapse/handlers/room_list.py b/synapse/handlers/room_list.py
index 0b7d3da68..59c9906b3 100644
--- a/synapse/handlers/room_list.py
+++ b/synapse/handlers/room_list.py
@@ -15,6 +15,7 @@
 
 import logging
 from collections import namedtuple
+from typing import Any, Dict, Optional
 
 from six import iteritems
 
@@ -105,22 +106,22 @@ class RoomListHandler(BaseHandler):
     @defer.inlineCallbacks
     def _get_public_room_list(
         self,
-        limit=None,
-        since_token=None,
-        search_filter=None,
-        network_tuple=EMPTY_THIRD_PARTY_ID,
-        from_federation=False,
-    ):
+        limit: Optional[int] = None,
+        since_token: Optional[str] = None,
+        search_filter: Optional[Dict] = None,
+        network_tuple: ThirdPartyInstanceID = EMPTY_THIRD_PARTY_ID,
+        from_federation: bool = False,
+    ) -> Dict[str, Any]:
         """Generate a public room list.
         Args:
-            limit (int|None): Maximum amount of rooms to return.
-            since_token (str|None)
-            search_filter (dict|None): Dictionary to filter rooms by.
-            network_tuple (ThirdPartyInstanceID): Which public list to use.
+            limit: Maximum amount of rooms to return.
+            since_token:
+            search_filter: Dictionary to filter rooms by.
+            network_tuple: Which public list to use.
                 This can be (None, None) to indicate the main list, or a particular
                 appservice and network id to use an appservice specific one.
                 Setting to None returns all public rooms across all lists.
-            from_federation (bool): Whether this request originated from a
+            from_federation: Whether this request originated from a
                 federating server or a client. Used for room filtering.
         """
 
diff --git a/synapse/rest/client/v1/room.py b/synapse/rest/client/v1/room.py
index bffd43de5..6b5830cc3 100644
--- a/synapse/rest/client/v1/room.py
+++ b/synapse/rest/client/v1/room.py
@@ -27,6 +27,7 @@ from synapse.api.constants import EventTypes, Membership
 from synapse.api.errors import (
     AuthError,
     Codes,
+    HttpResponseException,
     InvalidClientCredentialsError,
     SynapseError,
 )
@@ -364,10 +365,13 @@ class PublicRoomListRestServlet(TransactionRestServlet):
             limit = None
 
         handler = self.hs.get_room_list_handler()
-        if server:
-            data = await handler.get_remote_public_room_list(
-                server, limit=limit, since_token=since_token
-            )
+        if server and server != self.hs.config.server_name:
+            try:
+                data = await handler.get_remote_public_room_list(
+                    server, limit=limit, since_token=since_token
+                )
+            except HttpResponseException as e:
+                raise e.to_synapse_error()
         else:
             data = await handler.get_local_public_room_list(
                 limit=limit, since_token=since_token
@@ -404,15 +408,18 @@ class PublicRoomListRestServlet(TransactionRestServlet):
             limit = None
 
         handler = self.hs.get_room_list_handler()
-        if server:
-            data = await handler.get_remote_public_room_list(
-                server,
-                limit=limit,
-                since_token=since_token,
-                search_filter=search_filter,
-                include_all_networks=include_all_networks,
-                third_party_instance_id=third_party_instance_id,
-            )
+        if server and server != self.hs.config.server_name:
+            try:
+                data = await handler.get_remote_public_room_list(
+                    server,
+                    limit=limit,
+                    since_token=since_token,
+                    search_filter=search_filter,
+                    include_all_networks=include_all_networks,
+                    third_party_instance_id=third_party_instance_id,
+                )
+            except HttpResponseException as e:
+                raise e.to_synapse_error()
         else:
             data = await handler.get_local_public_room_list(
                 limit=limit,