diff --git a/lib/galaxy/managers/base.py b/lib/galaxy/managers/base.py
index 298ebc0b2b3..10b507250c7 100644
--- a/lib/galaxy/managers/base.py
+++ b/lib/galaxy/managers/base.py
@@ -576,8 +576,6 @@ class ModelSerializer(HasAModelManager[T]):
         keys_to_serialize = [ 'id', 'name', 'attr1', 'attr2', ... ]
         item_dict = MySerializer.serialize( my_item, keys_to_serialize )
     """
-    #: 'service' to use for getting urls - use class var to allow overriding when testing
-    url_for = staticmethod(gx_url_for)
     default_view: Optional[str]
     views: Dict[str, List[str]]
 
@@ -604,6 +602,12 @@ class ModelSerializer(HasAModelManager[T]):
         self.views = {}
         self.default_view = None
 
+    @staticmethod
+    def url_for(*args, context=None, **kwargs):
+        trans = context and context.get('trans')
+        url_for = trans and trans.url_builder or gx_url_for
+        return url_for(*args, **kwargs)
+
     def add_serializers(self):
         """
         Register a map of attribute keys -> serializing functions that will serialize
diff --git a/lib/galaxy/managers/datasets.py b/lib/galaxy/managers/datasets.py
index cf3bd0128bf..08358d9d49b 100644
--- a/lib/galaxy/managers/datasets.py
+++ b/lib/galaxy/managers/datasets.py
@@ -527,10 +527,11 @@ class _UnflattenedMetadataDatasetAssociationSerializer(base.ModelSerializer[T],
             if getattr(dataset_assoc.metadata, meta_type, None):
                 meta_files.append(
                     dict(file_type=meta_type,
-                         download_url=self.url_for('history_contents_metadata_file',
+                         download_url=self.url_for('get_metadata_file',
                                                    history_id=self.app.security.encode_id(dataset_assoc.history_id),
                                                    history_content_id=self.app.security.encode_id(dataset_assoc.id),
-                                                   metadata_file=meta_type)))
+                                                   query_params={'metadata_file': meta_type},
+                                                   context=context)))
         return meta_files
 
     def serialize_metadata(self, item, key, excluded=None, **context):
diff --git a/lib/galaxy/managers/hdas.py b/lib/galaxy/managers/hdas.py
index fd59c1585a9..4eca4e0d202 100644
--- a/lib/galaxy/managers/hdas.py
+++ b/lib/galaxy/managers/hdas.py
@@ -427,13 +427,15 @@ class HDASerializer(  # datasets._UnflattenedMetadataDatasetAssociationSerialize
             #   see also: https://sentry.galaxyproject.org/galaxy/galaxy-main/group/20769/events/9352883/
             'url': lambda item, key, **context: self.url_for('history_content',
                                                              history_id=self.app.security.encode_id(item.history_id),
-                                                             id=self.app.security.encode_id(item.id)),
+                                                             id=self.app.security.encode_id(item.id),
+                                                             context=context),
             'urls': self.serialize_urls,
 
             # TODO: backwards compat: need to go away
             'download_url': lambda item, key, **context: self.url_for('history_contents_display',
                                                                       history_id=self.app.security.encode_id(item.history.id),
-                                                                      history_content_id=self.app.security.encode_id(item.id)),
+                                                                      history_content_id=self.app.security.encode_id(item.id),
+                                                                      context=context),
             'parent_id': self.serialize_id,
             # TODO: to DatasetAssociationSerializer
             'accessible': lambda item, key, user=None, **c: self.manager.is_accessible(item, user, **c),
diff --git a/lib/galaxy/webapps/base/webapp.py b/lib/galaxy/webapps/base/webapp.py
index 9a99007f1af..e16a0aaba4b 100644
--- a/lib/galaxy/webapps/base/webapp.py
+++ b/lib/galaxy/webapps/base/webapp.py
@@ -192,7 +192,8 @@ def config_allows_origin(origin_raw, config):
 
 
 def url_builder(*args, **kwargs) -> str:
-    """Wrapper around the uWSGI version of the function for reversing URLs."""
+    """Wrapper around the WSGI version of the function for reversing URLs."""
+    kwargs.update(kwargs.pop('query_params', {}))
     return url_for(*args, **kwargs)
 
 
diff --git a/lib/galaxy/webapps/galaxy/api/__init__.py b/lib/galaxy/webapps/galaxy/api/__init__.py
index bc08740bc52..49ea15124b5 100644
--- a/lib/galaxy/webapps/galaxy/api/__init__.py
+++ b/lib/galaxy/webapps/galaxy/api/__init__.py
@@ -10,6 +10,7 @@ from typing import (
     Type,
     TypeVar,
 )
+from urllib.parse import urlencode
 
 from fastapi import (
     Cookie,
@@ -149,12 +150,20 @@ class UrlBuilder:
 
     def __call__(self, name: str, **path_params):
         qualified = path_params.pop("qualified", False)
+        # starlette does not support query parameters in url_path_for: https://github.com/encode/starlette/issues/560
+        query_params = path_params.pop('query_params', None)
         try:
             if qualified:
-                return self.request.url_for(name, **path_params)
-            return self.request.app.url_path_for(name, **path_params)
+                url = self.request.url_for(name, **path_params)
+            else:
+                url = self.request.app.url_path_for(name, **path_params)
+            if query_params:
+                url = f"{url}?{urlencode(query_params)}"
+            return url
         except NoMatchFound:
             # Fallback to legacy url_for
+            if query_params:
+                path_params.update(query_params)
             return web.url_for(name, **path_params)
 
 
diff --git a/lib/galaxy/webapps/galaxy/buildapp.py b/lib/galaxy/webapps/galaxy/buildapp.py
index 7a1f3989a00..44b08ca5c8b 100644
--- a/lib/galaxy/webapps/galaxy/buildapp.py
+++ b/lib/galaxy/webapps/galaxy/buildapp.py
@@ -297,7 +297,7 @@ def populate_api_routes(webapp, app):
                           controller='datasets',
                           action='show_inheritance_chain',
                           conditions=dict(method=["GET"]))
-    webapp.mapper.connect("history_contents_metadata_file",
+    webapp.mapper.connect("get_metadata_file",
                           "/api/histories/{history_id}/contents/{history_content_id}/metadata_file",
                           controller="datasets",
                           action="get_metadata_file",