diff --git a/lib/vagrant/env.rb b/lib/vagrant/env.rb
index d4ffcfd18..1560cc460 100644
--- a/lib/vagrant/env.rb
+++ b/lib/vagrant/env.rb
@@ -28,10 +28,9 @@ module Vagrant
       end
 
       def load_config!
-        load_paths = [
-          File.join(PROJECT_ROOT, "config", "default.rb"),
-          File.join(root_path, ROOTFILE_NAME)
-        ]
+        load_paths = [File.join(PROJECT_ROOT, "config", "default.rb")]
+        load_paths << File.join(box.directory, ROOTFILE_NAME) if box
+        load_paths << File.join(root_path, ROOTFILE_NAME)
 
         load_paths.each do |path|
           logger.info "Loading config from #{path}..."
@@ -59,6 +58,11 @@ module Vagrant
 
       def load_box!
         @@box = Box.find(Vagrant.config.vm.box) if Vagrant.config.vm.box
+
+        if @@box
+          logger.info("Reloading configuration to account for loaded box...")
+          load_config!
+        end
       end
 
       def load_vm!
diff --git a/test/vagrant/env_test.rb b/test/vagrant/env_test.rb
index e028ccdd9..37ac4c33e 100644
--- a/test/vagrant/env_test.rb
+++ b/test/vagrant/env_test.rb
@@ -57,6 +57,7 @@ class EnvTest < Test::Unit::TestCase
     setup do
       @root_path = "/foo"
       Vagrant::Env.stubs(:root_path).returns(@root_path)
+      Vagrant::Env.stubs(:box).returns(nil)
       File.stubs(:exist?).returns(false)
       Vagrant::Config.stubs(:execute!)
       Vagrant::Config.stubs(:reset!)
@@ -77,6 +78,20 @@ class EnvTest < Test::Unit::TestCase
       Vagrant::Env.load_config!
     end
 
+    should "not load from the box directory if it is nil" do
+      Vagrant::Env.expects(:box).once.returns(nil)
+      Vagrant::Env.load_config!
+    end
+
+    should "load from the box directory if it is not nil" do
+      dir = "foo"
+      box = mock("box")
+      box.stubs(:directory).returns(dir)
+      Vagrant::Env.expects(:box).twice.returns(box)
+      File.expects(:exist?).with(File.join(dir, Vagrant::Env::ROOTFILE_NAME)).once
+      Vagrant::Env.load_config!
+    end
+
     should "load the files only if exist? returns true" do
       File.expects(:exist?).once.returns(true)
       Vagrant::Env.expects(:load).once
@@ -102,6 +117,7 @@ class EnvTest < Test::Unit::TestCase
       Vagrant::Env.expects(:load_vm!).once
       Vagrant::Env.expects(:load_root_path!).once
       Vagrant::Env.expects(:load_home_directory!).once
+      Vagrant::Env.expects(:load_box!).once
       Vagrant::Env.load!
     end
   end
@@ -209,6 +225,8 @@ class EnvTest < Test::Unit::TestCase
   context "loading box" do
     setup do
       @box = mock("box")
+
+      Vagrant::Env.stubs(:load_config!)
     end
 
     should "set the box to what is found by the Box class" do
@@ -216,6 +234,18 @@ class EnvTest < Test::Unit::TestCase
       Vagrant::Env.load_box!
       assert @box.equal?(Vagrant::Env.box)
     end
+
+    should "load the config if a box is loaded" do
+      Vagrant::Env.expects(:load_config!).once
+      Vagrant::Box.expects(:find).returns(@box)
+      Vagrant::Env.load_box!
+    end
+
+    should "not load the config if a box is not loaded" do
+      Vagrant::Env.expects(:load_config!).never
+      Vagrant::Box.expects(:find).returns(nil)
+      Vagrant::Env.load_box!
+    end
   end
 
   context "requiring boxes" do