diff --git a/django/core/management/validation.py b/django/core/management/validation.py
index 2040a14582..a6d6a76985 100644
--- a/django/core/management/validation.py
+++ b/django/core/management/validation.py
@@ -113,6 +113,8 @@ def get_validation_errors(outfile, app=None):
                 e.add(opts, '"%s": BooleanFields do not accept null values. Use a NullBooleanField instead.' % f.name)
             if isinstance(f, models.FilePathField) and not (f.allow_files or f.allow_folders):
                 e.add(opts, '"%s": FilePathFields must have either allow_files or allow_folders set to True.' % f.name)
+            if isinstance(f, models.GenericIPAddressField) and not getattr(f, 'null', False) and getattr(f, 'blank', False):
+                e.add(opts, '"%s": GenericIPAddressField can not accept blank values if null values are not allowed, as blank values are stored as null.' % f.name)
             if f.choices:
                 if isinstance(f.choices, six.string_types) or not is_iterable(f.choices):
                     e.add(opts, '"%s": "choices" should be iterable (e.g., a tuple or list).' % f.name)
diff --git a/docs/releases/1.6.txt b/docs/releases/1.6.txt
index c01128c684..efc1297265 100644
--- a/docs/releases/1.6.txt
+++ b/docs/releases/1.6.txt
@@ -601,6 +601,13 @@ Miscellaneous
   ``django.contrib.admindocs.middleware`` because it is an implementation
   detail of admindocs, proven not to be reusable in general.
 
+* :class:`~django.db.models.GenericIPAddressField` will now only allow
+  ``blank`` values if ``null`` values are also allowed. Creating a
+  ``GenericIPAddressField`` where ``blank`` is allowed but ``null`` is not
+  will trigger a model validation error because ``blank`` values are always
+  stored as ``null``. Previously, storing a ``blank`` value in a field which
+  did not allow ``null`` would cause a database exception at runtime.
+
 Features deprecated in 1.6
 ==========================
 
diff --git a/tests/invalid_models/invalid_models/models.py b/tests/invalid_models/invalid_models/models.py
index 6ba3f04e5e..e1bac9cfb2 100644
--- a/tests/invalid_models/invalid_models/models.py
+++ b/tests/invalid_models/invalid_models/models.py
@@ -25,6 +25,7 @@ class FieldErrors(models.Model):
     index = models.CharField(max_length=10, db_index='bad')
     field_ = models.CharField(max_length=10)
     nullbool = models.BooleanField(null=True)
+    generic_ip_notnull_blank = models.GenericIPAddressField(null=False, blank=True)
 
 
 class Target(models.Model):
@@ -380,6 +381,7 @@ invalid_models.fielderrors: "choices2": "choices" should be a sequence of two-it
 invalid_models.fielderrors: "index": "db_index" should be either None, True or False.
 invalid_models.fielderrors: "field_": Field names cannot end with underscores, because this would lead to ambiguous queryset filters.
 invalid_models.fielderrors: "nullbool": BooleanFields do not accept null values. Use a NullBooleanField instead.
+invalid_models.fielderrors: "generic_ip_notnull_blank": GenericIPAddressField can not accept blank values if null values are not allowed, as blank values are stored as null.
 invalid_models.clash1: Accessor for field 'foreign' clashes with field 'Target.clash1_set'. Add a related_name argument to the definition for 'foreign'.
 invalid_models.clash1: Accessor for field 'foreign' clashes with related m2m field 'Target.clash1_set'. Add a related_name argument to the definition for 'foreign'.
 invalid_models.clash1: Reverse query name for field 'foreign' clashes with field 'Target.clash1'. Add a related_name argument to the definition for 'foreign'.
diff --git a/tests/validation/models.py b/tests/validation/models.py
index db083290fb..e95a1e0744 100644
--- a/tests/validation/models.py
+++ b/tests/validation/models.py
@@ -95,7 +95,7 @@ class GenericIPAddressTestModel(models.Model):
             blank=True, null=True)
 
 class GenericIPAddrUnpackUniqueTest(models.Model):
-    generic_v4unpack_ip = models.GenericIPAddressField(blank=True, unique=True, unpack_ipv4=True)
+    generic_v4unpack_ip = models.GenericIPAddressField(null=True, blank=True, unique=True, unpack_ipv4=True)
 
 
 # A model can't have multiple AutoFields
diff --git a/tests/validation/tests.py b/tests/validation/tests.py
index b571e0c298..9ddf796c2b 100644
--- a/tests/validation/tests.py
+++ b/tests/validation/tests.py
@@ -109,9 +109,9 @@ class GenericIPAddressFieldTests(ValidationTestCase):
 
     def test_correct_generic_ip_passes(self):
         giptm = GenericIPAddressTestModel(generic_ip="1.2.3.4")
-        self.assertEqual(None, giptm.full_clean())
+        self.assertIsNone(giptm.full_clean())
         giptm = GenericIPAddressTestModel(generic_ip="2001::2")
-        self.assertEqual(None, giptm.full_clean())
+        self.assertIsNone(giptm.full_clean())
 
     def test_invalid_generic_ip_raises_error(self):
         giptm = GenericIPAddressTestModel(generic_ip="294.4.2.1")
@@ -121,7 +121,7 @@ class GenericIPAddressFieldTests(ValidationTestCase):
 
     def test_correct_v4_ip_passes(self):
         giptm = GenericIPAddressTestModel(v4_ip="1.2.3.4")
-        self.assertEqual(None, giptm.full_clean())
+        self.assertIsNone(giptm.full_clean())
 
     def test_invalid_v4_ip_raises_error(self):
         giptm = GenericIPAddressTestModel(v4_ip="294.4.2.1")
@@ -131,7 +131,7 @@ class GenericIPAddressFieldTests(ValidationTestCase):
 
     def test_correct_v6_ip_passes(self):
         giptm = GenericIPAddressTestModel(v6_ip="2001::2")
-        self.assertEqual(None, giptm.full_clean())
+        self.assertIsNone(giptm.full_clean())
 
     def test_invalid_v6_ip_raises_error(self):
         giptm = GenericIPAddressTestModel(v6_ip="1.2.3.4")
@@ -151,10 +151,16 @@ class GenericIPAddressFieldTests(ValidationTestCase):
         giptm = GenericIPAddressTestModel(generic_ip="::ffff:10.10.10.10")
         giptm.save()
         giptm = GenericIPAddressTestModel(generic_ip="10.10.10.10")
-        self.assertEqual(None, giptm.full_clean())
+        self.assertIsNone(giptm.full_clean())
 
         # These two are the same, because we are doing IPv4 unpacking
         giptm = GenericIPAddrUnpackUniqueTest(generic_v4unpack_ip="::ffff:18.52.18.52")
         giptm.save()
         giptm = GenericIPAddrUnpackUniqueTest(generic_v4unpack_ip="18.52.18.52")
         self.assertFailsValidation(giptm.full_clean, ['generic_v4unpack_ip',])
+
+    def test_empty_generic_ip_passes(self):
+        giptm = GenericIPAddressTestModel(generic_ip="")
+        self.assertIsNone(giptm.full_clean())
+        giptm = GenericIPAddressTestModel(generic_ip=None)
+        self.assertIsNone(giptm.full_clean())