diff --git a/spec/gutter-container-spec.coffee b/spec/gutter-container-spec.coffee
index 03c9ebc10..e38367835 100644
--- a/spec/gutter-container-spec.coffee
+++ b/spec/gutter-container-spec.coffee
@@ -50,3 +50,13 @@ describe 'GutterContainer', ->
       otherGutterContainer = new GutterContainer fakeOtherTextEditor
       gutter = new Gutter 'gutter-name', otherGutterContainer
       expect(gutterContainer.removeGutter.bind(null, gutter)).toThrow()
+
+  describe '::destroy', ->
+    it 'clears its array of gutters and destroys custom gutters', ->
+      newGutter = gutterContainer.addGutter {'test-gutter', priority: 1}
+      newGutterSpy = jasmine.createSpy()
+      newGutter.onDidDestroy(newGutterSpy)
+
+      gutterContainer.destroy()
+      expect(newGutterSpy).toHaveBeenCalled()
+      expect(gutterContainer.getGutters()).toEqual []
diff --git a/src/gutter-container.coffee b/src/gutter-container.coffee
index 1be52d519..4fa7c61fb 100644
--- a/src/gutter-container.coffee
+++ b/src/gutter-container.coffee
@@ -13,7 +13,12 @@ class GutterContainer
     @emitter = new Emitter
 
   destroy: ->
-    @gutters = null
+    # Create a copy, because `Gutter::destroy` removes the gutter from
+    # GutterContainer's @gutters.
+    guttersToDestroy = @gutters.slice(0)
+    for gutter in guttersToDestroy
+      gutter.destroy() if gutter.name isnt 'line-number'
+    @gutters = []
     @emitter.dispose()
 
   # Creates and returns a {Gutter}.