diff --git a/django/contrib/auth/tests/custom_user.py b/django/contrib/auth/tests/custom_user.py
index 8cc57d4caf0..0d324f09539 100644
--- a/django/contrib/auth/tests/custom_user.py
+++ b/django/contrib/auth/tests/custom_user.py
@@ -144,3 +144,25 @@ class IsActiveTestUser1(AbstractBaseUser):
         app_label = 'auth'
 
     # the is_active attr is provided by AbstractBaseUser
+
+
+class CustomUserNonUniqueUsername(AbstractBaseUser):
+    "A user with a non-unique username"
+    username = models.CharField(max_length=30)
+
+    USERNAME_FIELD = 'username'
+
+    class Meta:
+        app_label = 'auth'
+
+
+class CustomUserBadRequiredFields(AbstractBaseUser):
+    "A user with a non-unique username"
+    username = models.CharField(max_length=30, unique=True)
+    date_of_birth = models.DateField()
+
+    USERNAME_FIELD = 'username'
+    REQUIRED_FIELDS = ['username', 'date_of_birth']
+
+    class Meta:
+        app_label = 'auth'
diff --git a/django/contrib/auth/tests/management.py b/django/contrib/auth/tests/management.py
index 42f14d6d5c9..687a5c31cbf 100644
--- a/django/contrib/auth/tests/management.py
+++ b/django/contrib/auth/tests/management.py
@@ -9,6 +9,8 @@ from django.contrib.auth.tests import CustomUser
 from django.contrib.auth.tests.utils import skipIfCustomUser
 from django.core.management import call_command
 from django.core.management.base import CommandError
+from django.core.management.validation import get_validation_errors
+from django.db.models.loading import get_app
 from django.test import TestCase
 from django.test.utils import override_settings
 from django.utils import six
@@ -170,6 +172,22 @@ class CreatesuperuserManagementCommandTestCase(TestCase):
         self.assertEqual(CustomUser._default_manager.count(), 0)
 
 
+class CustomUserModelValidationTestCase(TestCase):
+    @override_settings(AUTH_USER_MODEL='auth.CustomUserBadRequiredFields')
+    def test_username_not_in_required_fields(self):
+        "USERNAME_FIELD should not appear in REQUIRED_FIELDS."
+        new_io = StringIO()
+        get_validation_errors(new_io, get_app('auth'))
+        self.assertIn("The field named as the USERNAME_FIELD should not be included in REQUIRED_FIELDS on a swappable User model.", new_io.getvalue())
+
+    @override_settings(AUTH_USER_MODEL='auth.CustomUserNonUniqueUsername')
+    def test_username_non_unique(self):
+        "A non-unique USERNAME_FIELD should raise a model validation error."
+        new_io = StringIO()
+        get_validation_errors(new_io, get_app('auth'))
+        self.assertIn("The USERNAME_FIELD must be unique. Add unique=True to the field parameters.", new_io.getvalue())
+
+
 class PermissionDuplicationTestCase(TestCase):
 
     def setUp(self):
diff --git a/django/core/management/validation.py b/django/core/management/validation.py
index f49a3c22325..587d3a0ad7c 100644
--- a/django/core/management/validation.py
+++ b/django/core/management/validation.py
@@ -49,12 +49,16 @@ def get_validation_errors(outfile, app=None):
             # No need to perform any other validation checks on a swapped model.
             continue
 
-        # This is the current User model. Check known validation problems with User models
+        # If this is the current User model, check known validation problems with User models
         if settings.AUTH_USER_MODEL == '%s.%s' % (opts.app_label, opts.object_name):
             # Check that the USERNAME FIELD isn't included in REQUIRED_FIELDS.
             if cls.USERNAME_FIELD in cls.REQUIRED_FIELDS:
                 e.add(opts, 'The field named as the USERNAME_FIELD should not be included in REQUIRED_FIELDS on a swappable User model.')
 
+            # Check that the username field is unique
+            if not opts.get_field(cls.USERNAME_FIELD).unique:
+                e.add(opts, 'The USERNAME_FIELD must be unique. Add unique=True to the field parameters.')
+
         # Model isn't swapped; do field-specific validation.
         for f in opts.local_fields:
             if f.name == 'id' and not f.primary_key and opts.pk.name == 'id':
diff --git a/docs/topics/auth/customizing.txt b/docs/topics/auth/customizing.txt
index 7f1eff66242..d1ce6eb7dcb 100644
--- a/docs/topics/auth/customizing.txt
+++ b/docs/topics/auth/customizing.txt
@@ -492,7 +492,10 @@ password resets. You must then provide some key implementation details:
         A string describing the name of the field on the User model that is
         used as the unique identifier. This will usually be a username of
         some kind, but it can also be an email address, or any other unique
-        identifier. In the following example, the field `identifier` is used
+        identifier. The field *must* be unique (i.e., have ``unique=True``
+        set in it's definition).
+
+        In the following example, the field `identifier` is used
         as the identifying field::
 
             class MyUser(AbstractBaseUser):