diff --git a/plugins/provisioners/puppet/config/puppet.rb b/plugins/provisioners/puppet/config/puppet.rb
index 56b7a4a0f..99b06face 100644
--- a/plugins/provisioners/puppet/config/puppet.rb
+++ b/plugins/provisioners/puppet/config/puppet.rb
@@ -59,24 +59,18 @@ module VagrantPlugins
         def finalize!
           super
 
-          if @environment_path == UNSET_VALUE
-            if @manifests_path == UNSET_VALUE
-              if 1  #If both are unset, assume 'environment' mode.
-                @environment_path = [:host, "environments"]
-              else
-                @manifests_path = [:host, "manifests"]
-              end
-            end
-
-            if @manifests_path != UNSET_VALUE && !@manifests_path.is_a?(Array)
-              @manifests_path = [:host, @manifests_path]
-            end
-          else
-            if @environment_path != UNSET_VALUE && !@environment_path.is_a?(Array)
-              @environment_path = [:host, @environment_path]
-            end
+          if @environment_path == UNSET_VALUE && @manifests_path == UNSET_VALUE
+            #If both are unset, assume 'manifests' mode for now. TBD: Switch to environments by default?
+            @manifests_path = [:host, "manifests"]
           end
 
+          # If the paths are just strings, assume they are 'host' paths (rather than guest)
+          if @environment_path != UNSET_VALUE && !@environment_path.is_a?(Array)
+            @environment_path = [:host, @environment_path]
+          end
+          if @manifests_path != UNSET_VALUE && !@manifests_path.is_a?(Array)
+            @manifests_path = [:host, @manifests_path]
+          end
           @hiera_config_path = nil if @hiera_config_path == UNSET_VALUE
 
           if @environment_path == UNSET_VALUE
@@ -86,8 +80,12 @@ module VagrantPlugins
           else
             @environment_path[0] = @environment_path[0].to_sym
             @environment  = "production" if @environment == UNSET_VALUE
-            @manifest_file = nil
-            @manifests_path = nil
+            if @manifests_path == UNSET_VALUE
+              @manifests_path = nil
+            end            
+            if @manifest_file == UNSET_VALUE
+              @manifest_file = nil
+            end
           end
 
           @binary_path        = nil     if @binary_path == UNSET_VALUE
@@ -118,10 +116,6 @@ module VagrantPlugins
           # Calculate the manifests and module paths based on env
           this_expanded_module_paths = expanded_module_paths(machine.env.root_path)
 
-          if environment_path != nil && manifests_path != nil
-              errors << I18n.t("vagrant.provisioners.puppet.environment_manifest_conflict")
-          end
-
           # Manifests path/file validation
           if manifests_path != nil && manifests_path[0].to_sym == :host
             expanded_path = Pathname.new(manifests_path[1]).
diff --git a/plugins/provisioners/puppet/provisioner/puppet.rb b/plugins/provisioners/puppet/provisioner/puppet.rb
index b205b6b79..e68f8fa85 100644
--- a/plugins/provisioners/puppet/provisioner/puppet.rb
+++ b/plugins/provisioners/puppet/provisioner/puppet.rb
@@ -39,8 +39,8 @@ module VagrantPlugins
                 File.expand_path(@config.environment_path[1], root_path),
                 environments_guest_path, folder_opts)
             end
-          else
-            # Non-Environment mode
+          end
+          if @config.manifest_file
             @manifest_file  = File.join(manifests_guest_path, @config.manifest_file)
             # Share the manifests directory with the guest
             if @config.manifests_path[0].to_sym == :host
@@ -63,8 +63,8 @@ module VagrantPlugins
               if type == :stdout
                 # Parse out the environment manifest path since puppet apply doesnt do that for us.
                 if data =~ /\s+manifest\s+=\s(.*)/
-                  @environment_manifest_path = $1
-                  @environment_manifest_path.gsub! '$basemodulepath:', "#{environments_guest_path}/#{@config.environment}/"
+                  @manifest_file = $1
+                  @manifest_file.gsub! '$basemodulepath:', "#{environments_guest_path}/#{@config.environment}/"
                 end
               end
             end
@@ -78,13 +78,17 @@ module VagrantPlugins
             @machine.guest.capability(:wait_for_reboot)
           end
 
+          # In environment mode we still need to specify a manifest file, if its not, use the one from env config if specified.
+          if !@manifest_file
+            @manifest_file = "#{environments_guest_path}/#{@config.environment}/manifests/site.pp"
+            parse_environment_metadata
+          end
           # Check that the shared folders are properly shared
           check = []
           if @config.manifests_path.is_a?(Array) && @config.manifests_path[0] == :host
             check << manifests_guest_path
           end
           if @config.environment_path.is_a?(Array) && @config.environment_path[0] == :host
-            @environment_manifest_path = "#{environments_guest_path}/#{@config.environment}/manifests/site.pp"
             check << environments_guest_path
           end
           @module_paths.each do |host_path, guest_path|
@@ -111,7 +115,6 @@ module VagrantPlugins
             @machine.communicate.upload(local_hiera_path, @hiera_config_path)
           end
 
-          parse_environment_metadata
           run_puppet_apply
         end
 
@@ -181,15 +184,14 @@ module VagrantPlugins
 
           options << "--detailed-exitcodes"
           if config.environment_path
-            options << " #{@environment_manifest_path}"
             options << "--environmentpath #{environments_guest_path}/"
             options << "--environment #{@config.environment}"
           else
             options << "--manifestdir #{manifests_guest_path}"
-            options << @manifest_file
           end
+
+          options << @manifest_file
           options = options.join(" ")
-          
           @machine.ui.info("Running ye puppet apply with options #{options}")
 
           # Build up the custom facts if we have any
diff --git a/templates/locales/en.yml b/templates/locales/en.yml
index 8ddc475db..f3782cdbf 100644
--- a/templates/locales/en.yml
+++ b/templates/locales/en.yml
@@ -1864,10 +1864,6 @@ en:
           Please specify a path to an existing Puppet directory environment.
         environment_path_missing: "The environment path specified for Puppet does not exist: %{path}"
         manifests_path_missing: "The manifests path specified for Puppet does not exist: %{path}"
-        environment_manifest_conflict: |-
-          You may not specify both environment_path and manifests_path. 
-          Please specify environment and environment_path without manifests_path, or
-          manifests_path without environment_path (deprecated).
         missing_shared_folders: |-
           Shared folders that Puppet requires are missing on the virtual machine.
           This is usually due to configuration changing after already booting the