diff --git a/middleman-core/features/helpers_auto_javascript_include_tag.feature b/middleman-core/features/helpers_auto_javascript_include_tag.feature
index 4407ea72..ffcf7df5 100644
--- a/middleman-core/features/helpers_auto_javascript_include_tag.feature
+++ b/middleman-core/features/helpers_auto_javascript_include_tag.feature
@@ -6,6 +6,11 @@ Feature: Built-in auto_javascript_include_tag view helper
     When I go to "/auto-js.html"
     Then I should see "javascripts/auto-js.js"
 
+  Scenario: Viewing the root path (directory index)
+    Given the Server is running at "auto-js-directory-index-app"
+    When I go to "/auto-js/index.html"
+    Then I should see "javascripts/auto-js.js"
+
   Scenario: Viewing the root path (build mode)
     Given a successfully built app at "auto-js-app"
     When I cd to "build"
diff --git a/middleman-core/fixtures/auto-js-directory-index-app/config.rb b/middleman-core/fixtures/auto-js-directory-index-app/config.rb
new file mode 100644
index 00000000..f343b291
--- /dev/null
+++ b/middleman-core/fixtures/auto-js-directory-index-app/config.rb
@@ -0,0 +1 @@
+activate :directory_indexes
\ No newline at end of file
diff --git a/middleman-core/fixtures/auto-js-directory-index-app/source/auto-js.html.erb b/middleman-core/fixtures/auto-js-directory-index-app/source/auto-js.html.erb
new file mode 100755
index 00000000..7af247d9
--- /dev/null
+++ b/middleman-core/fixtures/auto-js-directory-index-app/source/auto-js.html.erb
@@ -0,0 +1 @@
+<%= auto_javascript_include_tag %>
\ No newline at end of file
diff --git a/middleman-core/fixtures/auto-js-directory-index-app/source/javascripts/auto-js.js b/middleman-core/fixtures/auto-js-directory-index-app/source/javascripts/auto-js.js
new file mode 100644
index 00000000..8b137891
--- /dev/null
+++ b/middleman-core/fixtures/auto-js-directory-index-app/source/javascripts/auto-js.js
@@ -0,0 +1 @@
+
diff --git a/middleman-core/lib/middleman-core/core_extensions/default_helpers.rb b/middleman-core/lib/middleman-core/core_extensions/default_helpers.rb
index fa359a77..8c6b0ca2 100644
--- a/middleman-core/lib/middleman-core/core_extensions/default_helpers.rb
+++ b/middleman-core/lib/middleman-core/core_extensions/default_helpers.rb
@@ -122,7 +122,7 @@ class Middleman::CoreExtensions::DefaultHelpers < ::Middleman::Extension
 
       # If the basename of the request as no extension, assume we are serving a
       # directory and join index_file to the path.
-      path = File.join(asset_dir, current_path)
+      path = File.join(asset_dir, current_resource.path)
       path = path.sub(/#{Regexp.escape(File.extname(path))}$/, ".#{asset_ext}")
 
       yield path if sitemap.find_resource_by_path(path)