diff --git a/netbox/ipam/api/views.py b/netbox/ipam/api/views.py
index 3c8f3c43d..0e975146a 100644
--- a/netbox/ipam/api/views.py
+++ b/netbox/ipam/api/views.py
@@ -96,28 +96,41 @@ class PrefixViewSet(CustomFieldModelViewSet):
             if not request.user.has_perm('ipam.add_ipaddress'):
                 raise PermissionDenied()
 
-            # Find the first available IP address in the prefix
-            try:
-                ipaddress = list(prefix.get_available_ips())[0]
-            except IndexError:
+            # Determine if the requested number of IPs is available
+            requested_count = len(request.data) if isinstance(request.data, list) else 1
+            available_ips = list(prefix.get_available_ips())
+            if len(available_ips) < requested_count:
                 return Response(
                     {
-                        "detail": "There are no available IPs within this prefix ({})".format(prefix)
+                        "detail": "An insufficient number of IP addresses are available within the prefix {} ({} "
+                                  "requested, {} available)".format(prefix, requested_count, len(available_ips))
                     },
                     status=status.HTTP_400_BAD_REQUEST
                 )
 
-            # Create the new IP address
-            data = request.data.copy()
-            data['address'] = '{}/{}'.format(ipaddress, prefix.prefix.prefixlen)
-            data['vrf'] = prefix.vrf.pk if prefix.vrf else None
-            serializer = serializers.WritableIPAddressSerializer(data=data)
+            # Deserializing multiple IP addresses
+            if isinstance(request.data, list):
+                request_data = list(request.data)  # Need a mutable copy
+                for obj in request_data:
+                    obj['address'] = available_ips.pop(0)
+                    obj['vrf'] = prefix.vrf.pk if prefix.vrf else None
+                serializer = serializers.WritableIPAddressSerializer(data=request_data, many=True)
+
+            # Deserializing a single IP address
+            else:
+                request_data = request.data.copy()  # Need a mutable copy
+                request_data['address'] = available_ips.pop(0)
+                request_data['vrf'] = prefix.vrf.pk if prefix.vrf else None
+                serializer = serializers.WritableIPAddressSerializer(data=request_data)
+
+            # Create the new IP address(es)
             if serializer.is_valid():
                 serializer.save()
                 return Response(serializer.data, status=status.HTTP_201_CREATED)
+
             return Response(serializer.errors, status=status.HTTP_400_BAD_REQUEST)
 
-        # Determine the maximum amount of IPs to return
+        # Determine the maximum number of IPs to return
         else:
             try:
                 limit = int(request.query_params.get('limit', settings.PAGINATE_COUNT))
diff --git a/netbox/ipam/tests/test_api.py b/netbox/ipam/tests/test_api.py
index cba624a59..b39116b9f 100644
--- a/netbox/ipam/tests/test_api.py
+++ b/netbox/ipam/tests/test_api.py
@@ -365,7 +365,7 @@ class PrefixTest(HttpStatusMixin, APITestCase):
         self.assertHttpStatus(response, status.HTTP_204_NO_CONTENT)
         self.assertEqual(Prefix.objects.count(), 2)
 
-    def test_available_ips(self):
+    def test_list_available_ips(self):
 
         prefix = Prefix.objects.create(prefix=IPNetwork('192.0.2.0/29'), is_pool=True)
         url = reverse('ipam-api:prefix-available-ips', kwargs={'pk': prefix.pk})
@@ -380,12 +380,19 @@ class PrefixTest(HttpStatusMixin, APITestCase):
         response = self.client.get(url, **self.header)
         self.assertEqual(len(response.data), 6)  # 8 - 2 because prefix.is_pool = False
 
-        # Create all six available IPs
-        for i in range(6):
+    def test_create_single_available_ip(self):
+
+        prefix = Prefix.objects.create(prefix=IPNetwork('192.0.2.0/30'), is_pool=True)
+        url = reverse('ipam-api:prefix-available-ips', kwargs={'pk': prefix.pk})
+
+        # Create all four available IPs with individual requests
+        for i in range(1, 5):
             data = {
                 'description': 'Test IP {}'.format(i)
             }
             response = self.client.post(url, data, **self.header)
+            if response.status_code != status.HTTP_201_CREATED:
+                assert False, response.content
             self.assertHttpStatus(response, status.HTTP_201_CREATED)
             self.assertEqual(response.data['description'], data['description'])
 
@@ -394,6 +401,27 @@ class PrefixTest(HttpStatusMixin, APITestCase):
         self.assertHttpStatus(response, status.HTTP_400_BAD_REQUEST)
         self.assertIn('detail', response.data)
 
+    def test_create_multiple_available_ips(self):
+
+        prefix = Prefix.objects.create(prefix=IPNetwork('192.0.2.0/29'), is_pool=True)
+        url = reverse('ipam-api:prefix-available-ips', kwargs={'pk': prefix.pk})
+
+        # Try to create nine IPs (only eight are available)
+        data = [{'description': 'Test IP {}'.format(i)} for i in range(1, 10)]  # 9 IPs
+        response = self.client.post(url, data, format='json', **self.header)
+        self.assertHttpStatus(response, status.HTTP_400_BAD_REQUEST)
+        self.assertIn('detail', response.data)
+
+        # Verify that no IPs were created (eight are still available)
+        response = self.client.get(url, **self.header)
+        self.assertEqual(len(response.data), 8)
+
+        # Create all eight available IPs in a single request
+        data = [{'description': 'Test IP {}'.format(i)} for i in range(1, 9)]  # 8 IPs
+        response = self.client.post(url, data, format='json', **self.header)
+        self.assertHttpStatus(response, status.HTTP_201_CREATED)
+        self.assertEqual(len(response.data), 8)
+
 
 class IPAddressTest(HttpStatusMixin, APITestCase):