diff --git a/django/contrib/admin/options.py b/django/contrib/admin/options.py
index d97597fe66dd..e93fdf40475d 100644
--- a/django/contrib/admin/options.py
+++ b/django/contrib/admin/options.py
@@ -475,24 +475,25 @@ def lookup_allowed(self, lookup, value, request=None):
                 # Lookups on nonexistent fields are ok, since they're ignored
                 # later.
                 break
+            if not prev_field or (
+                prev_field.is_relation
+                and field not in model._meta.parents.values()
+                and field is not model._meta.auto_field
+                and (
+                    model._meta.auto_field is None
+                    or part not in getattr(prev_field, "to_fields", [])
+                )
+                and (field.is_relation or not field.primary_key)
+            ):
+                relation_parts.append(part)
             if not getattr(field, "path_infos", None):
                 # This is not a relational field, so further parts
                 # must be transforms.
                 break
-            if (
-                not prev_field
-                or (field.is_relation and field not in model._meta.parents.values())
-                or (
-                    prev_field.is_relation
-                    and model._meta.auto_field is None
-                    and part not in getattr(prev_field, "to_fields", [])
-                )
-            ):
-                relation_parts.append(part)
             prev_field = field
             model = field.path_infos[-1].to_opts.model
 
-        if not relation_parts or len(parts) == 1:
+        if len(relation_parts) <= 1:
             # Either a local field filter, or no fields at all.
             return True
         valid_lookups = {self.date_hierarchy}
diff --git a/docs/releases/5.0.3.txt b/docs/releases/5.0.3.txt
index 30e87127b0b7..b433bf6f2fe7 100644
--- a/docs/releases/5.0.3.txt
+++ b/docs/releases/5.0.3.txt
@@ -15,3 +15,8 @@ Bugfixes
 * Fixed a bug in Django 5.0 that caused a crash of ``Signal.asend()`` and
   ``asend_robust()`` when all receivers were asynchronous functions
   (:ticket:`35174`).
+
+* Fixed a regression in Django 5.0.1 where :meth:`.ModelAdmin.lookup_allowed`
+  would prevent filtering against foreign keys using lookups like ``__isnull``
+  when the field was not included in :attr:`.ModelAdmin.list_filter`
+  (:ticket:`35173`).
diff --git a/tests/modeladmin/tests.py b/tests/modeladmin/tests.py
index fad2dfaa1cde..de8d26ae4657 100644
--- a/tests/modeladmin/tests.py
+++ b/tests/modeladmin/tests.py
@@ -174,7 +174,19 @@ class PlaceAdmin(ModelAdmin):
             pass
 
         ma = PlaceAdmin(Place, self.site)
-        self.assertIs(ma.lookup_allowed("country", "1", request), True)
+
+        cases = [
+            ("country", "1"),
+            ("country__exact", "1"),
+            ("country__id", "1"),
+            ("country__id__exact", "1"),
+            ("country__isnull", True),
+            ("country__isnull", False),
+            ("country__id__isnull", False),
+        ]
+        for lookup, lookup_value in cases:
+            with self.subTest(lookup=lookup):
+                self.assertIs(ma.lookup_allowed(lookup, lookup_value, request), True)
 
     @isolate_apps("modeladmin")
     def test_lookup_allowed_non_autofield_primary_key(self):