diff --git a/spec/app/editor-spec.coffee b/spec/app/editor-spec.coffee
index d30a3b3f2..a9cf99230 100644
--- a/spec/app/editor-spec.coffee
+++ b/spec/app/editor-spec.coffee
@@ -1863,6 +1863,19 @@ describe "Editor", ->
           expect(editor.renderedLines.find('.line:eq(10) .indent-guide').length).toBe 2
           expect(editor.renderedLines.find('.line:eq(10) .indent-guide').text()).toBe '    '
 
+      describe "when a line contains only whitespace", ->
+        it "displays an indent guide on the line", ->
+          editor.attachToDom()
+          config.set("editor.showIndentGuide", true)
+
+          editor.setCursorBufferPosition([10])
+          editor.indent()
+          console.log 'here'
+          editor.indent()
+          expect(editor.getCursorBufferPosition()).toEqual [10, 4]
+          expect(editor.renderedLines.find('.line:eq(10) .indent-guide').length).toBe 2
+          expect(editor.renderedLines.find('.line:eq(10) .indent-guide').text()).toBe '    '
+
   describe "gutter rendering", ->
     beforeEach ->
       editor.attachToDom(heightInLines: 5.5)
diff --git a/src/app/editor.coffee b/src/app/editor.coffee
index 3631e1cd6..b85c88479 100644
--- a/src/app/editor.coffee
+++ b/src/app/editor.coffee
@@ -1201,16 +1201,14 @@ class Editor extends View
     else
       firstNonWhitespacePosition = screenLine.text.search(/\S/)
       firstTrailingWhitespacePosition = screenLine.text.search(/\s*$/)
+      lineIsWhitespaceOnly = firstTrailingWhitespacePosition is 0
       position = 0
       for token in screenLine.tokens
         updateScopeStack(token.scopes)
-        line.push(token.getValueAsHtml(
-          invisibles: invisibles
-          hasLeadingWhitespace: position < firstNonWhitespacePosition
-          hasTrailingWhitespace: position + token.value.length > firstTrailingWhitespacePosition
-          hasIndentGuide: @showIndentGuide
-        ))
-
+        hasLeadingWhitespace =  position < firstNonWhitespacePosition
+        hasTrailingWhitespace = position + token.value.length > firstTrailingWhitespacePosition
+        hasIndentGuide = @showIndentGuide and (hasLeadingWhitespace or lineIsWhitespaceOnly)
+        line.push(token.getValueAsHtml({invisibles, hasLeadingWhitespace, hasTrailingWhitespace, hasIndentGuide}))
         position += token.value.length
 
     popScope() while scopeStack.length > 0
diff --git a/src/app/token.coffee b/src/app/token.coffee
index fa3f0dc6b..1bcd45660 100644
--- a/src/app/token.coffee
+++ b/src/app/token.coffee
@@ -92,6 +92,7 @@ class Token
         html = html.replace /[ ]+$/, (match) ->
           classes = []
           classes.push('invisible') if invisibles.space
+          classes.push('indent-guide') if hasIndentGuide
           classes.push('trailing-whitespace')
           match = match.replace(/./g, invisibles.space) if invisibles.space
           "<span class='#{classes.join(' ')}'>#{match}</span>"