diff --git a/src/browser/atom-application.coffee b/src/browser/atom-application.coffee
index 3255b0a19..d08990264 100644
--- a/src/browser/atom-application.coffee
+++ b/src/browser/atom-application.coffee
@@ -174,9 +174,6 @@ class AtomApplication
     @on 'application:quit', -> app.quit()
     @on 'application:new-window', -> @openPath(getLoadSettings())
     @on 'application:new-file', -> (@focusedWindow() ? this).openPath()
-    @on 'application:open', -> @promptForPathToOpen('all', getLoadSettings())
-    @on 'application:open-file', -> @promptForPathToOpen('file', getLoadSettings())
-    @on 'application:open-folder', -> @promptForPathToOpen('folder', getLoadSettings())
     @on 'application:open-dev', -> @promptForPathToOpen('all', devMode: true)
     @on 'application:open-safe', -> @promptForPathToOpen('all', safeMode: true)
     @on 'application:inspect', ({x, y, atomWindow}) ->
@@ -259,6 +256,14 @@ class AtomApplication
     ipcMain.on 'command', (event, command) =>
       @emit(command)
 
+    ipcMain.on 'open-command', (event, command, args...) =>
+      defaultPath = args[0] if args.length > 0
+      switch command
+        when 'application:open' then @promptForPathToOpen('all', getLoadSettings(), defaultPath)
+        when 'application:open-file' then @promptForPathToOpen('file', getLoadSettings(), defaultPath)
+        when 'application:open-folder' then @promptForPathToOpen('folder', getLoadSettings(), defaultPath)
+        else console.log "Invalid open-command received: " + command
+
     ipcMain.on 'window-command', (event, command, args...) ->
       win = BrowserWindow.fromWebContents(event.sender)
       win.emit(command, args...)
@@ -657,11 +662,13 @@ class AtomApplication
   #   :safeMode - A Boolean which controls whether any newly opened windows
   #               should be in safe mode or not.
   #   :window - An {AtomWindow} to use for opening a selected file path.
-  promptForPathToOpen: (type, {devMode, safeMode, window}) ->
-    @promptForPath type, (pathsToOpen) =>
-      @openPaths({pathsToOpen, devMode, safeMode, window})
+  #   :path - An optional String which controls the default path to which the
+  #           file dialog opens.
+  promptForPathToOpen: (type, {devMode, safeMode, window}, path=null) ->
+    @promptForPath type, ((pathsToOpen) =>
+      @openPaths({pathsToOpen, devMode, safeMode, window})), path
 
-  promptForPath: (type, callback) ->
+  promptForPath: (type, callback, path) ->
     properties =
       switch type
         when 'file' then ['openFile']
@@ -684,8 +691,8 @@ class AtomApplication
         when 'folder' then 'Open Folder'
         else 'Open'
 
-    if process.platform is 'linux'
-      if projectPath = @lastFocusedWindow?.projectPath
-        openOptions.defaultPath = projectPath
+    # File dialog defaults to project directory of currently active editor
+    if path?
+      openOptions.defaultPath = path
 
     dialog.showOpenDialog(parentWindow, openOptions, callback)
diff --git a/src/register-default-commands.coffee b/src/register-default-commands.coffee
index 1cb3d99b5..1fff6f633 100644
--- a/src/register-default-commands.coffee
+++ b/src/register-default-commands.coffee
@@ -31,9 +31,15 @@ module.exports = ({commandRegistry, commandInstaller, config, notificationManage
     'application:unhide-all-applications': -> ipcRenderer.send('command', 'application:unhide-all-applications')
     'application:new-window': -> ipcRenderer.send('command', 'application:new-window')
     'application:new-file': -> ipcRenderer.send('command', 'application:new-file')
-    'application:open': -> ipcRenderer.send('command', 'application:open')
-    'application:open-file': -> ipcRenderer.send('command', 'application:open-file')
-    'application:open-folder': -> ipcRenderer.send('command', 'application:open-folder')
+    'application:open': ->
+      defaultPath = atom.workspace.getActiveTextEditor()?.getPath() ? atom.project.getPaths()?[0]
+      ipcRenderer.send('open-command', 'application:open', defaultPath)
+    'application:open-file': ->
+      defaultPath = atom.workspace.getActiveTextEditor()?.getPath() ? atom.project.getPaths()?[0]
+      ipcRenderer.send('open-command', 'application:open-file', defaultPath)
+    'application:open-folder': ->
+      defaultPath = atom.workspace.getActiveTextEditor()?.getPath() ? atom.project.getPaths()?[0]
+      ipcRenderer.send('open-command', 'application:open-folder', defaultPath)
     'application:open-dev': -> ipcRenderer.send('command', 'application:open-dev')
     'application:open-safe': -> ipcRenderer.send('command', 'application:open-safe')
     'application:add-project-folder': -> atom.addProjectFolder()