diff --git a/spec/text-editor-component-spec.coffee b/spec/text-editor-component-spec.coffee
index 35c58512e..cc35b51b1 100644
--- a/spec/text-editor-component-spec.coffee
+++ b/spec/text-editor-component-spec.coffee
@@ -374,6 +374,22 @@ describe "TextEditorComponent", ->
         expect(line2LeafNodes[2].textContent).toBe '  '
         expect(line2LeafNodes[2].classList.contains('indent-guide')).toBe true
 
+      it "renders indent guides correctly on lines containing only whitespace when invisibles are enabled", ->
+        atom.config.set 'editor.showInvisibles', true
+        atom.config.set 'editor.invisibles', space: '-', eol: 'x'
+        editor.getBuffer().insert([1, Infinity], '\n      ')
+        nextAnimationFrame()
+
+        line2LeafNodes = getLeafNodes(component.lineNodeForScreenRow(2))
+        expect(line2LeafNodes.length).toBe 4
+        expect(line2LeafNodes[0].textContent).toBe '--'
+        expect(line2LeafNodes[0].classList.contains('indent-guide')).toBe true
+        expect(line2LeafNodes[1].textContent).toBe '--'
+        expect(line2LeafNodes[1].classList.contains('indent-guide')).toBe true
+        expect(line2LeafNodes[2].textContent).toBe '--'
+        expect(line2LeafNodes[2].classList.contains('indent-guide')).toBe true
+        expect(line2LeafNodes[3].textContent).toBe 'x'
+
       it "does not render indent guides in trailing whitespace for lines containing non whitespace characters", ->
         editor.getBuffer().setText "  hi  "
         nextAnimationFrame()
diff --git a/src/lines-component.coffee b/src/lines-component.coffee
index ff8827a21..6099de185 100644
--- a/src/lines-component.coffee
+++ b/src/lines-component.coffee
@@ -213,8 +213,7 @@ LinesComponent = React.createClass
     innerHTML = ""
 
     scopeStack = []
-    firstTrailingWhitespacePosition = text.search(/\s*$/)
-    lineIsWhitespaceOnly = firstTrailingWhitespacePosition is 0
+    lineIsWhitespaceOnly = line.isOnlyWhitespace()
     for token in tokens
       innerHTML += @updateScopeStack(scopeStack, token.scopes)
       hasIndentGuide = not editor.isMini() and showIndentGuide and (token.hasLeadingWhitespace() or (token.hasTrailingWhitespace() and lineIsWhitespaceOnly))
diff --git a/src/tokenized-line.coffee b/src/tokenized-line.coffee
index 60eab31d9..2e9a6a7e7 100644
--- a/src/tokenized-line.coffee
+++ b/src/tokenized-line.coffee
@@ -9,6 +9,7 @@ idCounter = 1
 module.exports =
 class TokenizedLine
   endOfLineInvisibles: null
+  lineIsWhitespaceOnly: false
 
   constructor: ({tokens, @lineEnding, @ruleStack, @startBufferColumn, @fold, @tabLength, @indentLevel, @invisibles}) ->
     @startBufferColumn ?= 0
@@ -146,7 +147,7 @@ class TokenizedLine
   markLeadingAndTrailingWhitespaceTokens: ->
     firstNonWhitespaceIndex = @text.search(NonWhitespaceRegex)
     firstTrailingWhitespaceIndex = @text.search(TrailingWhitespaceRegex)
-    lineIsWhitespaceOnly = firstTrailingWhitespaceIndex is 0
+    @lineIsWhitespaceOnly = firstTrailingWhitespaceIndex is 0
     index = 0
     for token in @tokens
       if index < firstNonWhitespaceIndex
@@ -202,12 +203,7 @@ class TokenizedLine
     false
 
   isOnlyWhitespace: ->
-    if @text == ''
-      true
-    else
-      for token in @tokens
-        return false unless token.isOnlyWhitespace()
-      true
+    @lineIsWhitespaceOnly
 
   tokenAtIndex: (index) ->
     @tokens[index]