diff --git a/lib/vagrant/errors.rb b/lib/vagrant/errors.rb
index ebdf23516..944bdd5f8 100644
--- a/lib/vagrant/errors.rb
+++ b/lib/vagrant/errors.rb
@@ -448,6 +448,10 @@ module Vagrant
       error_key(:not_found, "vagrant.actions.vm.host_only_network")
     end
 
+    class NetworkTypeNotSupported < VagrantError
+      error_key(:network_type_not_supported)
+    end
+
     class NFSBadExports < VagrantError
       error_key(:nfs_bad_exports)
     end
diff --git a/plugins/guests/darwin/cap/configure_networks.rb b/plugins/guests/darwin/cap/configure_networks.rb
index 1be71c82f..36487cd08 100644
--- a/plugins/guests/darwin/cap/configure_networks.rb
+++ b/plugins/guests/darwin/cap/configure_networks.rb
@@ -35,12 +35,19 @@ module VagrantPlugins
             end
 
             network_type = network[:type].to_sym
-            if network_type == :static
-              command = "networksetup -setmanual \"#{service_name}\" #{network[:ip]} #{network[:netmask]}"
-            elsif network_type == :dhcp
+            case network_type.to_sym
+            when :static
+              command = "networksetup -setmanual \"#{service_name}\" #{network[:ip]} #{network[:netmask]} #{network[:router]}"
+            when :static6
+              command = "networksetup -setv6manual \"#{service_name}\" #{network[:ip]} #{network[:netmask]} #{network[:router]}"
+            when :dhcp
               command = "networksetup -setdhcp \"#{service_name}\""
+            when :dhcp6
+              # This is not actually possible yet in Vagrant, but when we do
+              # enable IPv6 across the board, Darwin will already have support.
+              command = "networksetup -setv6automatic \"#{service_name}\""
             else
-              raise "#{network_type} network type is not supported, try static or dhcp"
+              raise Vagrant::Errors::NetworkTypeNotSupported, type: network_type
             end
 
             machine.communicate.sudo(command)
@@ -65,7 +72,7 @@ module VagrantPlugins
           ints = ::IO.read(tmp_ints)
           ints.split(/\n\n/m).each do |i|
             if i.match(/Hardware/) && i.match(/Ethernet/)
-              # Ethernet, should be 2 lines, 
+              # Ethernet, should be 2 lines,
               # (3) Thunderbolt Ethernet
               # (Hardware Port: Thunderbolt Ethernet, Device: en1)
 
diff --git a/templates/locales/en.yml b/templates/locales/en.yml
index fc3d6245c..d3fa33e13 100755
--- a/templates/locales/en.yml
+++ b/templates/locales/en.yml
@@ -869,6 +869,8 @@ en:
         If the problem persists, please report a bug to the net-ssh project.
 
         %{message}
+      network_type_not_supported: |-
+        The %{type} network type is not supported for this box or guest.
       nfs_bad_exports: |-
         NFS is reporting that your exports file is invalid. Vagrant does
         this check before making any changes to the file. Please correct