diff --git a/django/contrib/admin/options.py b/django/contrib/admin/options.py
index b045b2df02..af69f4cb3b 100644
--- a/django/contrib/admin/options.py
+++ b/django/contrib/admin/options.py
@@ -474,24 +474,24 @@ class BaseModelAdmin(metaclass=forms.MediaDefiningClass):
                 # 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", [])
-                )
-            ):
-                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 len(relation_parts) <= 1:
+        if not relation_parts:
             # Either a local field filter, or no fields at all.
             return True
         valid_lookups = {self.date_hierarchy}
diff --git a/docs/releases/5.0.1.txt b/docs/releases/5.0.1.txt
index f1b6e0f8bb..871f55ec6d 100644
--- a/docs/releases/5.0.1.txt
+++ b/docs/releases/5.0.1.txt
@@ -9,4 +9,6 @@ Django 5.0.1 fixes several bugs in 5.0.
 Bugfixes
 ========
 
-* ...
+* Reallowed, following a regression in Django 5.0, using a foreign key to a
+  model with a primary key that is not ``AutoField`` in
+  :attr:`.ModelAdmin.list_filter` (:ticket:`35020`).
diff --git a/tests/modeladmin/tests.py b/tests/modeladmin/tests.py
index ec46b04c2e..e0c4d6e727 100644
--- a/tests/modeladmin/tests.py
+++ b/tests/modeladmin/tests.py
@@ -162,6 +162,20 @@ class ModelAdminTests(TestCase):
             True,
         )
 
+    @isolate_apps("modeladmin")
+    def test_lookup_allowed_non_autofield_primary_key(self):
+        class Country(models.Model):
+            id = models.CharField(max_length=2, primary_key=True)
+
+        class Place(models.Model):
+            country = models.ForeignKey(Country, models.CASCADE)
+
+        class PlaceAdmin(ModelAdmin):
+            list_filter = ["country"]
+
+        ma = PlaceAdmin(Place, self.site)
+        self.assertIs(ma.lookup_allowed("country__id__exact", "DE", request), True)
+
     @isolate_apps("modeladmin")
     def test_lookup_allowed_foreign_primary(self):
         class Country(models.Model):