diff --git a/lib/vagrant/environment.rb b/lib/vagrant/environment.rb
index dfd07b720..74019d42a 100644
--- a/lib/vagrant/environment.rb
+++ b/lib/vagrant/environment.rb
@@ -32,7 +32,7 @@ module Vagrant
       def check_virtualbox!
         version = VirtualBox.version
         raise Errors::VirtualBoxNotDetected if version.nil?
-        raise Errors::VirtualBoxInvalidVersion, :version => version.to_s if version.to_f < 3.2
+        raise Errors::VirtualBoxInvalidVersion, :version => version.to_s if version.to_f < 4.0
         raise Errors::VirtualBoxInvalidOSE, :version => version.to_s if version.to_s.downcase.include?("ose")
       rescue Errors::VirtualBoxNotDetected
         # On 64-bit Windows, show a special error. This error is a subclass
diff --git a/templates/locales/en.yml b/templates/locales/en.yml
index 485d450a9..05dbfc333 100644
--- a/templates/locales/en.yml
+++ b/templates/locales/en.yml
@@ -96,8 +96,13 @@ en:
         to continue.
       virtualbox_invalid_version: |-
         Vagrant has detected that you have VirtualBox version %{version} installed!
-        Vagrant requires that you use at least VirtualBox version 3.2. Please install
+        Vagrant requires that you use at least VirtualBox version 4.0. Please install
         a more recent version of VirtualBox to continue.
+
+        The Vagrant 0.6.x series supports VirtualBox 3.2, so if you're stuck with that
+        version, then please use the 0.6.x series of Vagrant.
+
+        Any earlier versions of VirtualBox are completely unsupported. Please upgrade.
       virtualbox_not_detected: |-
         Vagrant could not detect VirtualBox! Make sure VirtualBox is properly installed.
         If VirtualBox is installed, it may be an incorrect version. Vagrant currently