diff --git a/synapse/handlers/profile.py b/synapse/handlers/profile.py
index ce044aa480..5c4a54b920 100644
--- a/synapse/handlers/profile.py
+++ b/synapse/handlers/profile.py
@@ -627,13 +627,23 @@ class ProfileHandler:
                 propagate=propagate,
             )
         else:
-            await self.set_profile_field(
-                target_user=target_user,
-                requester=requester,
-                field_name=field_name,
-                new_value=new_value,
-                by_admin=by_admin,
-            )
+            # For custom fields, we need to call a separate delete method
+            # for empty strings.
+            if new_value == "":
+                await self.delete_profile_field(
+                    target_user=target_user,
+                    requester=requester,
+                    field_name=field_name,
+                    by_admin=by_admin,
+                )
+            else:
+                await self.set_profile_field(
+                    target_user=target_user,
+                    requester=requester,
+                    field_name=field_name,
+                    new_value=new_value,
+                    by_admin=by_admin,
+                )
 
     async def set_profile_field(
         self,
diff --git a/synapse/replication/http/profile.py b/synapse/replication/http/profile.py
index 93b7be2d07..c5e5448f8e 100644
--- a/synapse/replication/http/profile.py
+++ b/synapse/replication/http/profile.py
@@ -63,7 +63,7 @@ class ReplicationProfileSetFieldValue(ReplicationEndpoint):
     async def _serialize_payload(  # type: ignore[override]
         requester_id: str,
         field_name: str,
-        new_value: str | None,
+        new_value: str,
         by_admin: bool = False,
         propagate: bool = False,
         authenticated_entity: str | None = None,
@@ -84,7 +84,9 @@ class ReplicationProfileSetFieldValue(ReplicationEndpoint):
         # ie an admin who has done the request on behalf of the user.
         requester = create_requester(
             user_id=user_id,
-            authenticated_entity=content["authenticated_entity"] if content["by_admin"] else None,
+            authenticated_entity=content["authenticated_entity"]
+            if content["by_admin"]
+            else None,
         )
         await self._profile_handler.set_field(
             target_user=UserID.from_string(user_id),
diff --git a/synapse/rest/client/profile.py b/synapse/rest/client/profile.py
index e7b2e4bcda..7cd4678bc0 100644
--- a/synapse/rest/client/profile.py
+++ b/synapse/rest/client/profile.py
@@ -241,12 +241,6 @@ class ProfileFieldRestServlet(RestServlet):
     async def on_DELETE(
         self, request: SynapseRequest, user_id: str, field_name: str
     ) -> tuple[int, JsonDict]:
-        if not self._is_profile_worker:
-            raise SynapseError(
-                HTTPStatus.METHOD_NOT_ALLOWED,
-                "Can only handle DELETE /profile on instances configured to handle the profile_updates stream writer",
-                Codes.UNRECOGNIZED,
-            )
         if not UserID.is_valid(user_id):
             raise SynapseError(
                 HTTPStatus.BAD_REQUEST, "Invalid user id", Codes.INVALID_PARAM
@@ -286,17 +280,32 @@ class ProfileFieldRestServlet(RestServlet):
                 Codes.USER_ACCOUNT_SUSPENDED,
             )
 
-        if field_name == ProfileFields.DISPLAYNAME:
-            await self.profile_handler.set_displayname(
-                user, requester, "", by_admin=is_admin, propagate=propagate
-            )
-        elif field_name == ProfileFields.AVATAR_URL:
-            await self.profile_handler.set_avatar_url(
-                user, requester, "", by_admin=is_admin, propagate=propagate
+        if self._is_profile_worker:
+            await self.profile_handler.set_field(
+                target_user=user,
+                requester=requester,
+                field_name=field_name,
+                new_value="",
+                by_admin=is_admin,
+                propagate=propagate,
             )
         else:
-            await self.profile_handler.delete_profile_field(
-                user, requester, field_name, by_admin=is_admin
+            # Offload to the right worker via http replication
+            set_profile_data_client = ReplicationProfileSetFieldValue.make_client(
+                self.hs
+            )
+            profile_updates_writer_instance = (
+                self.hs.config.worker.writers.profile_updates[0]
+            )
+            await set_profile_data_client(
+                instance_name=profile_updates_writer_instance,
+                user_id=user.to_string(),
+                requester_id=requester.user.to_string(),
+                field_name=field_name,
+                new_value="",
+                by_admin=is_admin,
+                propagate=propagate,
+                authenticated_entity=requester.authenticated_entity,
             )
 
         return 200, {}