diff --git a/plugins/commands/login/middleware/add_authentication.rb b/plugins/commands/login/middleware/add_authentication.rb
index a784a3ac6..3056a88f9 100644
--- a/plugins/commands/login/middleware/add_authentication.rb
+++ b/plugins/commands/login/middleware/add_authentication.rb
@@ -7,6 +7,7 @@ module VagrantPlugins
   module LoginCommand
     class AddAuthentication
       ALLOWED_AUTHENTICATION_HOSTS = %w[
+        app.vagrantup.com
         atlas.hashicorp.com
         vagrantcloud.com
       ].freeze
diff --git a/test/unit/plugins/commands/login/middleware/add_authentication_test.rb b/test/unit/plugins/commands/login/middleware/add_authentication_test.rb
index ee4b2ab7d..8f1d1c6d9 100644
--- a/test/unit/plugins/commands/login/middleware/add_authentication_test.rb
+++ b/test/unit/plugins/commands/login/middleware/add_authentication_test.rb
@@ -71,13 +71,15 @@ describe VagrantPlugins::LoginCommand::AddAuthentication do
 
       original = [
         "http://google.com/box.box",
+        "http://app.vagrantup.com/foo.box",
         "http://vagrantcloud.com/foo.box",
         "http://vagrantcloud.com/bar.box?arg=true",
       ]
 
       expected = original.dup
       expected[1] = "#{original[1]}?access_token=#{token}"
-      expected[2] = "#{original[2]}&access_token=#{token}"
+      expected[2] = "#{original[2]}?access_token=#{token}"
+      expected[3] = "#{original[3]}&access_token=#{token}"
 
       env[:box_urls] = original.dup
       subject.call(env)