diff --git a/spec/editor-view-spec.coffee b/spec/editor-view-spec.coffee
index d324001b0..23804de70 100644
--- a/spec/editor-view-spec.coffee
+++ b/spec/editor-view-spec.coffee
@@ -1829,6 +1829,21 @@ describe "EditorView", ->
       expect(editorView.gutter.find('.line-number:eq(3)')).not.toHaveClass 'foldable'
       expect(editorView.gutter.find('.line-number:eq(4)')).toHaveClass 'foldable'
 
+      # changes to indentation update foldability
+      editor.setIndentationForBufferRow(1, 0)
+      expect(editorView.gutter.find('.line-number:eq(0)')).not.toHaveClass 'foldable'
+      expect(editorView.gutter.find('.line-number:eq(1)')).toHaveClass 'foldable'
+
+      # changes to comments update foldability
+      editor.toggleLineCommentsForBufferRows(2, 3)
+      expect(editorView.gutter.find('.line-number:eq(2)')).toHaveClass 'foldable'
+      expect(editorView.gutter.find('.line-number:eq(3)')).not.toHaveClass 'foldable'
+      editor.toggleLineCommentForBufferRow(2)
+      expect(editorView.gutter.find('.line-number:eq(2)')).not.toHaveClass 'foldable'
+      expect(editorView.gutter.find('.line-number:eq(3)')).not.toHaveClass 'foldable'
+      editor.toggleLineCommentForBufferRow(4)
+      expect(editorView.gutter.find('.line-number:eq(3)')).toHaveClass 'foldable'
+
     describe "when lines are inserted", ->
       it "re-renders the correct line number range in the gutter", ->
         editorView.scrollTop(3 * editorView.lineHeight)
diff --git a/src/gutter.coffee b/src/gutter.coffee
index 3cddd9e61..c1097cc51 100644
--- a/src/gutter.coffee
+++ b/src/gutter.coffee
@@ -151,10 +151,12 @@ class Gutter extends View
           updateAllLines = true
           break
 
+    # If a change added or removed lines, just rebuild the entire gutter
     if updateAllLines
       @lineNumbers[0].innerHTML = @buildLineElementsHtml(startScreenRow, endScreenRow)
+
+    # Handle changes that didn't add/remove lines more optimally
     else
-      # When scrolling or adding/removing lines, we just add/remove lines from the ends.
       if startScreenRow < @firstScreenRow
         @prependLineElements(@buildLineElements(startScreenRow, @firstScreenRow-1))
       else if startScreenRow != @firstScreenRow
@@ -165,6 +167,8 @@ class Gutter extends View
       else if endScreenRow != @lastScreenRow
         @removeLineElements(endScreenRow - @lastScreenRow)
 
+      @updateFoldableClasses(changes)
+
     @firstScreenRow = startScreenRow
     @lastScreenRow = endScreenRow
     @highlightedRows = null
@@ -219,6 +223,23 @@ class Gutter extends View
 
     html
 
+  # Private: Called to update the 'foldable' class of line numbers when there's
+  # a change to the display buffer that doesn't regenerate all the line numbers
+  # anyway.
+  updateFoldableClasses: (changes) ->
+    editor = @getEditor()
+    for {start, end} in changes when start <= @lastScreenRow
+      startScreenRow = Math.max(start - 1, @firstScreenRow)
+      endScreenRow =  Math.min(end + 1, @lastScreenRow)
+      lastBufferRow = null
+      for bufferRow in editor.bufferRowsForScreenRows(startScreenRow, endScreenRow) when bufferRow isnt lastBufferRow
+        lastBufferRow = bufferRow
+        lineNumberElement = @getLineNumberElement(bufferRow)[0]
+        if editor.isFoldableAtBufferRow(bufferRow)
+          lineNumberElement.classList.add('foldable')
+        else
+          lineNumberElement.classList.remove('foldable')
+
   removeLineHighlights: ->
     return unless @highlightedLineNumbers
     for line in @highlightedLineNumbers