diff --git a/spec/app/file-finder-spec.coffee b/spec/app/file-finder-spec.coffee
index 9f06aeb9c..3ffbb42a3 100644
--- a/spec/app/file-finder-spec.coffee
+++ b/spec/app/file-finder-spec.coffee
@@ -94,23 +94,3 @@ describe 'FileFinder', ->
     it "returns paths sorted by score of match against the given query", ->
       expect(finder.findMatches('ap')).toEqual ["app.coffee", "atom/app.coffee"]
       expect(finder.findMatches('a/ap')).toEqual ["atom/app.coffee"]
-
-  describe "when it is removed", ->
-    input = null
-
-    beforeEach ->
-      input = $$ -> @input value : "this has focus"
-      input.attachToDom()
-      input.focus()
-      expect(document.activeElement).toBe input[0]
-
-      finder = new FileFinder(paths: [])
-      finder.attachToDom()
-      expect(document.activeElement).not.toBe input[0]
-
-    afterEach ->
-      input.remove()
-
-    it "returns focus to previous active element", ->
-      finder.remove()
-      expect(document.activeElement).toBe input[0]
diff --git a/spec/app/root-view-spec.coffee b/spec/app/root-view-spec.coffee
index 0bc567a48..264f0c6ca 100644
--- a/spec/app/root-view-spec.coffee
+++ b/spec/app/root-view-spec.coffee
@@ -44,6 +44,7 @@ describe "RootView", ->
       delete atom.windowStatesByWindowNumber[$windowNumber]
 
     it "stores its window state on the atom object by window number, then reassigns it next time the root view is constructed", ->
+      rootView.activeEditor().splitLeft()
       expectedWindowState = rootView.getWindowState()
 
       # simulate unload
@@ -52,7 +53,9 @@ describe "RootView", ->
 
       # simulate reload
       newRootView = new RootView
+
       expect(newRootView.getWindowState()).toEqual expectedWindowState
+      expect(newRootView.editors.length).toBe 2
 
   describe "focus", ->
     it "can receive focus if there is no active editor, but otherwise hands off focus to the active editor", ->
@@ -81,6 +84,8 @@ describe "RootView", ->
       editor3.setCursorScreenPosition([2, 3])
       editor4.setBuffer(new Buffer(require.resolve 'fixtures/sample.txt'))
       editor4.setCursorScreenPosition([0, 2])
+      rootView.attachToDom()
+      editor2.focus()
       panesHtml = rootView.panes.html()
 
     it "can reconstruct the split pane arrangement from the window state hash returned by getWindowState", ->
@@ -112,6 +117,12 @@ describe "RootView", ->
       expect(editor3.width()).toBeGreaterThan 0
       expect(editor4.width()).toBeGreaterThan 0
 
+      # ensure correct editor is focused again
+      expect(editor2.isFocused).toBeTruthy()
+      expect(editor1.isFocused).toBeFalsy()
+      expect(editor3.isFocused).toBeFalsy()
+      expect(editor4.isFocused).toBeFalsy()
+
 
   describe "split editor panes", ->
     editor1 = null
diff --git a/src/app/editor.coffee b/src/app/editor.coffee
index 5292d567f..b50abd3e3 100644
--- a/src/app/editor.coffee
+++ b/src/app/editor.coffee
@@ -168,7 +168,7 @@ class Editor extends View
       @calculateDimensions()
       @hiddenInput.width(@charWidth)
       @setMaxLineLength() if @softWrap
-      @focus()
+      @focus() if @isFocused
 
   rootView: ->
     @parents('#root-view').view()
@@ -227,12 +227,14 @@ class Editor extends View
     buffer = editorState.buffer ? new Buffer
     @editorStatesByBufferId[buffer.id] = editorState
     @setBuffer(buffer)
+    @isFocused = editorState.isFocused
 
   getEditorState: ->
     buffer: @buffer
     cursorScreenPosition: @getCursorScreenPosition().copy()
     scrollTop: @scroller.scrollTop()
     scrollLeft: @scroller.scrollLeft()
+    isFocused: @isFocused
 
   saveEditorStateForCurrentBuffer: ->
     @editorStatesByBufferId[@buffer.id] = @getEditorState()
diff --git a/src/app/file-finder.coffee b/src/app/file-finder.coffee
index a1cf9c165..c7f006bd7 100644
--- a/src/app/file-finder.coffee
+++ b/src/app/file-finder.coffee
@@ -16,7 +16,6 @@ class FileFinder extends View
   initialize: ({@paths, @selected}) ->
     requireStylesheet 'file-finder.css'
     @maxResults = 10
-    @previousFocusedElement = $(document.activeElement)
 
     @populatePathList()
 
@@ -44,10 +43,6 @@ class FileFinder extends View
     @selected(filePath) if filePath and @selected
     @remove()
 
-  remove: ->
-    super()
-    @previousFocusedElement.focus()
-
   moveUp: ->
     @findSelectedLi()
       .filter(':not(:first-child)')
diff --git a/src/app/root-view.coffee b/src/app/root-view.coffee
index aacbd959b..1b9b10db2 100644
--- a/src/app/root-view.coffee
+++ b/src/app/root-view.coffee
@@ -192,3 +192,4 @@ class RootView extends View
           paths: relativePaths
           selected: (relativePath) => @open(relativePath)
         @append @fileFinder
+        @fileFinder.editor.focus()