diff --git a/synapse/appservice/api.py b/synapse/appservice/api.py
index 8651134ce4..cf9ab28bec 100644
--- a/synapse/appservice/api.py
+++ b/synapse/appservice/api.py
@@ -268,6 +268,7 @@ class ApplicationServiceApi(SimpleHttpClient):
         user_id: str,
         from_user_id: Optional[UserID] = None,
         key: Optional[str] = None,
+        origin_server: Optional[str] = None,
     ) -> Optional[JsonDict]:
         if service.url is None:
             return None
@@ -281,6 +282,8 @@ class ApplicationServiceApi(SimpleHttpClient):
                 args["access_token"] = service.hs_token
             if from_user_id:
                 args["from_user_id"] = from_user_id.to_string()
+            if origin_server:
+                args["origin_server"] = origin_server
 
             url = f"{service.url}{APP_SERVICE_PREFIX}/profile/{urllib.parse.quote(user_id)}"
 
diff --git a/synapse/handlers/appservice.py b/synapse/handlers/appservice.py
index a0b5738ca0..2259e82f54 100644
--- a/synapse/handlers/appservice.py
+++ b/synapse/handlers/appservice.py
@@ -737,7 +737,7 @@ class ApplicationServicesHandler:
         return False
 
     async def query_profile(
-        self, user_id: str, from_user_id: Optional[UserID] = None, key: Optional[str] = None
+        self, user_id: str, from_user_id: Optional[UserID] = None, key: Optional[str] = None, origin_server: Optional[str] = None
     ) -> Optional[JsonDict]:
         """Check if any application service knows this user_id exists.
 
@@ -751,7 +751,7 @@ class ApplicationServicesHandler:
         for user_service in user_query_services:
             if user_service.supports_profile_lookup:
                 profile = await self.appservice_api.query_profile(
-                    user_service, user_id, from_user_id, key
+                    user_service, user_id, from_user_id, key, origin_server
                 )
                 if profile:
                     accumulated_profile.update(profile)
diff --git a/synapse/handlers/profile.py b/synapse/handlers/profile.py
index eb03a875a1..3029918665 100644
--- a/synapse/handlers/profile.py
+++ b/synapse/handlers/profile.py
@@ -139,6 +139,8 @@ class ProfileHandler:
                 raise e.to_synapse_error()
 
         # Check whether the appservice has any information about the user.
+
+        logger.info(f"query_profile {user_id} {from_user_id}")
         as_profile = await self._as.query_profile(user_id, from_user_id)
         ret.update(as_profile)
 
@@ -464,6 +466,7 @@ class ProfileHandler:
             The value for the profile field or None if the field does not exist.
         """
 
+        logger.info(f"get_profile_field {field_name} {from_user_id}")
         # Check whether the appservice has any information about the user.
         as_profile = await self._as.query_profile(
             target_user.to_string(), from_user_id, field_name
@@ -576,9 +579,12 @@ class ProfileHandler:
             raise SynapseError(400, "User is not hosted on this homeserver")
 
         just_field = args.get("field")
+        origin_server = args.get("origin")
+
+        assert origin_server
 
         # Check whether the appservice has any information about the user.
-        as_profile = await self._as.query_profile(user.to_string(), key=just_field)
+        as_profile = await self._as.query_profile(user.to_string(), key=just_field, origin_server=origin_server)
         if just_field and just_field in as_profile:
             return as_profile[just_field]
 
diff --git a/synapse/rest/client/profile.py b/synapse/rest/client/profile.py
index db1aa64cbb..0e5d6af76e 100644
--- a/synapse/rest/client/profile.py
+++ b/synapse/rest/client/profile.py
@@ -113,11 +113,8 @@ class ProfileFieldRestServlet(RestServlet):
     async def on_GET(
         self, request: SynapseRequest, user_id: str, field_name: str
     ) -> Tuple[int, JsonDict]:
-        requester_user = None
-
-        if self.hs.config.server.require_auth_for_profile_requests:
-            requester = await self.auth.get_user_by_req(request)
-            requester_user = requester.user
+        requester = await self.auth.get_user_by_req(request)
+        requester_user = requester.user
 
         if not UserID.is_valid(user_id):
             raise SynapseError(
@@ -137,7 +134,7 @@ class ProfileFieldRestServlet(RestServlet):
             )
 
         user = UserID.from_string(user_id)
-        await self.profile_handler.check_profile_query_allowed(user, requester_user)
+        await self.profile_handler.check_profile_query_allowed(user, requester_user if self.hs.config.server.require_auth_for_profile_requests else None)
 
         if field_name == ProfileFields.DISPLAYNAME:
             field_value: JsonValue = await self.profile_handler.get_displayname(