diff --git a/src/atom.coffee b/src/atom.coffee
index d497d1701..f208c3f92 100644
--- a/src/atom.coffee
+++ b/src/atom.coffee
@@ -308,6 +308,9 @@ class Atom extends Model
     @themes.loadBaseStylesheets()
     @packages.loadPackages()
     @deserializeEditorWindow()
+
+    @watchProjectPath()
+
     @packages.activate()
     @keymaps.loadUserKeymap()
     @requireUserInitScript()
@@ -347,6 +350,13 @@ class Atom extends Model
         pack.reloadStylesheets?()
       null
 
+  # Notify the browser project of the window's current project path
+  watchProjectPath: ->
+    onProjectPathChanged = =>
+      ipc.send('window-command', 'project-path-changed', @project.getPath())
+    @subscribe @project, 'path-changed', onProjectPathChanged
+    onProjectPathChanged()
+
   # Public: Open a new Atom window using the given options.
   #
   # Calling this method without an options parameter will open a prompt to pick
diff --git a/src/browser/atom-application.coffee b/src/browser/atom-application.coffee
index 624359ba9..81c561778 100644
--- a/src/browser/atom-application.coffee
+++ b/src/browser/atom-application.coffee
@@ -327,9 +327,17 @@ class AtomApplication
     {pathToOpen, initialLine, initialColumn} = @locationForPathToOpen(pathToOpen)
 
     unless pidToKillWhenClosed or newWindow
-      # Open files in the specified window or the last focused window
-      if fs.statSyncNoException(pathToOpen).isFile?()
-        existingWindow = window ? @topWindow
+      pathToOpenStat = fs.statSyncNoException(pathToOpen)
+
+      # Default to using the specified window or the last focused window
+      currentWindow = window ? @topWindow
+
+      if pathToOpenStat.isFile?()
+        # Open the file in the current window
+        existingWindow = currentWindow
+      else if pathToOpenStat.isDirectory?()
+        # Open the folder in the current window if it doesn't have a path
+        existingWindow = currentWindow unless currentWindow?.hasProjectPath()
 
       # Don't reuse windows in dev mode
       existingWindow ?= @windowForPath(pathToOpen) unless devMode
diff --git a/src/browser/atom-window.coffee b/src/browser/atom-window.coffee
index 04d647ba6..4958dd782 100644
--- a/src/browser/atom-window.coffee
+++ b/src/browser/atom-window.coffee
@@ -49,6 +49,8 @@ class AtomWindow
       @emit 'window:loaded'
       @loaded = true
 
+    @browserWindow.on 'project-path-changed', (@projectPath) =>
+
     @browserWindow.loadUrl @getUrl(loadSettings)
     @browserWindow.focusOnWebView() if @isSpec
 
@@ -66,6 +68,8 @@ class AtomWindow
       slashes: true
       query: {loadSettings: JSON.stringify(loadSettings)}
 
+  hasProjectPath: -> @projectPath?.length > 0
+
   getInitialPath: ->
     @browserWindow.loadSettings.initialPath
 
diff --git a/src/window-event-handler.coffee b/src/window-event-handler.coffee
index bdf50bd4b..5f2b09b62 100644
--- a/src/window-event-handler.coffee
+++ b/src/window-event-handler.coffee
@@ -28,7 +28,9 @@ class WindowEventHandler
     @subscribe $(window), 'blur', -> document.body.classList.add('is-blurred')
 
     @subscribe $(window), 'window:open-path', (event, {pathToOpen, initialLine, initialColumn}) ->
-      unless fs.isDirectorySync(pathToOpen)
+      if fs.isDirectorySync(pathToOpen)
+        atom.project.setPath(pathToOpen) unless atom.project.getPath()
+      else
         atom.workspace?.open(pathToOpen, {initialLine, initialColumn})
 
     @subscribe $(window), 'beforeunload', =>