diff --git a/django/contrib/auth/forms.py b/django/contrib/auth/forms.py
index 0376d177094..eaae0bf6953 100644
--- a/django/contrib/auth/forms.py
+++ b/django/contrib/auth/forms.py
@@ -147,16 +147,22 @@ class BaseUserCreationForm(forms.ModelForm):
 
 
 class UserCreationForm(BaseUserCreationForm):
-    error_messages = {
-        **BaseUserCreationForm.error_messages,
-        "unique": _("A user with that username already exists."),
-    }
-
     def clean_username(self):
         """Reject usernames that differ only in case."""
         username = self.cleaned_data.get("username")
-        if username and User.objects.filter(username__iexact=username).exists():
-            raise forms.ValidationError(self.error_messages["unique"], code="unique")
+        if (
+            username
+            and self._meta.model.objects.filter(username__iexact=username).exists()
+        ):
+            self._update_errors(
+                ValidationError(
+                    {
+                        "username": self.instance.unique_error_message(
+                            self._meta.model, ["username"]
+                        )
+                    }
+                )
+            )
         else:
             return username
 
diff --git a/django/contrib/auth/locale/en/LC_MESSAGES/django.po b/django/contrib/auth/locale/en/LC_MESSAGES/django.po
index bc6eff91dd1..8b15915f9fa 100644
--- a/django/contrib/auth/locale/en/LC_MESSAGES/django.po
+++ b/django/contrib/auth/locale/en/LC_MESSAGES/django.po
@@ -77,10 +77,6 @@ msgstr ""
 msgid "Enter the same password as before, for verification."
 msgstr ""
 
-#: contrib/auth/forms.py:152 contrib/auth/models.py:353
-msgid "A user with that username already exists."
-msgstr ""
-
 #: contrib/auth/forms.py:168
 msgid ""
 "Raw passwords are not stored, so there is no way to see this user’s "
@@ -240,6 +236,10 @@ msgstr ""
 msgid "Required. 150 characters or fewer. Letters, digits and @/./+/-/_ only."
 msgstr ""
 
+#: contrib/auth/models.py:353
+msgid "A user with that username already exists."
+msgstr ""
+
 #: contrib/auth/models.py:356
 msgid "first name"
 msgstr ""
diff --git a/tests/auth_tests/test_forms.py b/tests/auth_tests/test_forms.py
index c3ce1f570ff..7a80adbf314 100644
--- a/tests/auth_tests/test_forms.py
+++ b/tests/auth_tests/test_forms.py
@@ -372,6 +372,35 @@ class UserCreationFormTest(TestDataMixin, TestCase):
             ["A user with that username already exists."],
         )
 
+    @override_settings(AUTH_USER_MODEL="auth_tests.ExtensionUser")
+    def test_case_insensitive_username_custom_user_and_error_message(self):
+        class CustomUserCreationForm(UserCreationForm):
+            class Meta(UserCreationForm.Meta):
+                model = ExtensionUser
+                fields = UserCreationForm.Meta.fields + ("date_of_birth",)
+                error_messages = {
+                    "username": {"unique": "This username has already been taken."}
+                }
+
+        ExtensionUser.objects.create_user(
+            username="testclient",
+            password="password",
+            email="testclient@example.com",
+            date_of_birth=datetime.date(1984, 3, 5),
+        )
+        data = {
+            "username": "TeStClIeNt",
+            "password1": "test123",
+            "password2": "test123",
+            "date_of_birth": "1980-01-01",
+        }
+        form = CustomUserCreationForm(data)
+        self.assertIs(form.is_valid(), False)
+        self.assertEqual(
+            form["username"].errors,
+            ["This username has already been taken."],
+        )
+
 
 # To verify that the login form rejects inactive users, use an authentication
 # backend that allows them.