diff --git a/django/contrib/admin/checks.py b/django/contrib/admin/checks.py
index 1665023434..aa43718cd6 100644
--- a/django/contrib/admin/checks.py
+++ b/django/contrib/admin/checks.py
@@ -532,7 +532,7 @@ class BaseModelAdminChecks:
                 field=field_name, option=label, obj=obj, id="admin.E019"
             )
         else:
-            if not field.many_to_many:
+            if not field.many_to_many or isinstance(field, models.ManyToManyRel):
                 return must_be(
                     "a many-to-many field", option=label, obj=obj, id="admin.E020"
                 )
diff --git a/docs/releases/5.0.1.txt b/docs/releases/5.0.1.txt
index 15b735b42e..4344b0d181 100644
--- a/docs/releases/5.0.1.txt
+++ b/docs/releases/5.0.1.txt
@@ -32,3 +32,7 @@ Bugfixes
 
 * Fixed a regression in Django 5.0 where querysets referenced incorrect field
   names from ``FilteredRelation()`` (:ticket:`35050`).
+
+* Fixed a regression in Django 5.0 that caused a system check crash when
+  ``ModelAdmin.filter_horizontal`` or ``filter_vertical`` contained a reverse
+  many-to-many relation with ``related_name`` (:ticket:`35056`).
diff --git a/tests/modeladmin/test_checks.py b/tests/modeladmin/test_checks.py
index 2ed27f8a3d..85c175d581 100644
--- a/tests/modeladmin/test_checks.py
+++ b/tests/modeladmin/test_checks.py
@@ -322,6 +322,24 @@ class FilterVerticalCheckTests(CheckTestCase):
             "admin.E020",
         )
 
+    @isolate_apps("modeladmin")
+    def test_invalid_reverse_m2m_field_with_related_name(self):
+        class Contact(Model):
+            pass
+
+        class Customer(Model):
+            contacts = ManyToManyField("Contact", related_name="customers")
+
+        class TestModelAdmin(ModelAdmin):
+            filter_vertical = ["customers"]
+
+        self.assertIsInvalid(
+            TestModelAdmin,
+            Contact,
+            "The value of 'filter_vertical[0]' must be a many-to-many field.",
+            "admin.E020",
+        )
+
     @isolate_apps("modeladmin")
     def test_invalid_m2m_field_with_through(self):
         class Artist(Model):
@@ -384,6 +402,24 @@ class FilterHorizontalCheckTests(CheckTestCase):
             "admin.E020",
         )
 
+    @isolate_apps("modeladmin")
+    def test_invalid_reverse_m2m_field_with_related_name(self):
+        class Contact(Model):
+            pass
+
+        class Customer(Model):
+            contacts = ManyToManyField("Contact", related_name="customers")
+
+        class TestModelAdmin(ModelAdmin):
+            filter_horizontal = ["customers"]
+
+        self.assertIsInvalid(
+            TestModelAdmin,
+            Contact,
+            "The value of 'filter_horizontal[0]' must be a many-to-many field.",
+            "admin.E020",
+        )
+
     @isolate_apps("modeladmin")
     def test_invalid_m2m_field_with_through(self):
         class Artist(Model):