diff --git a/spec/text-editor-component-spec.coffee b/spec/text-editor-component-spec.coffee
index bfc343c03..3e3de2928 100644
--- a/spec/text-editor-component-spec.coffee
+++ b/spec/text-editor-component-spec.coffee
@@ -2713,26 +2713,35 @@ describe "TextEditorComponent", ->
         expect(line1LeafNodes[1].classList.contains('indent-guide')).toBe false
 
   describe "middle mouse paste on Linux", ->
-    it "pastes the previously selected text", ->
+    originalPlatform = null
+
+    beforeEach ->
+      originalPlatform = process.platform
+      Object.defineProperty process, 'platform', value: 'linux'
+
+    afterEach ->
+      Object.defineProperty process, 'platform', value: originalPlatform
+
+    it "pastes the previously selected text at the clicked location", ->
+      jasmine.unspy(window, 'setTimeout')
+      clipboardWrittenTo = false
       spyOn(require('ipc'), 'send').andCallFake (eventName, selectedText) ->
         if eventName is 'write-text-to-selection-clipboard'
           require('clipboard').writeText(selectedText, 'selection')
+          clipboardWrittenTo = true
 
       atom.clipboard.write('')
-      component.listenForMiddleMousePaste()
-
-      editor.setCursorBufferPosition([10, 0])
-      componentNode.querySelector('.scroll-view').dispatchEvent(buildMouseEvent('mouseup', which: 2))
-
-      expect(atom.clipboard.read()).toBe ''
-      expect(editor.lineTextForBufferRow(10)).toBe ''
-
+      component.trackSelectionClipboard()
       editor.setSelectedBufferRange([[1, 6], [1, 10]])
-      editor.setCursorBufferPosition([10, 0])
-      componentNode.querySelector('.scroll-view').dispatchEvent(buildMouseEvent('mouseup', which: 2))
 
-      expect(atom.clipboard.read()).toBe 'sort'
-      expect(editor.lineTextForBufferRow(10)).toBe 'sort'
+      waitsFor ->
+        clipboardWrittenTo
+
+      runs ->
+        componentNode.querySelector('.scroll-view').dispatchEvent(buildMouseEvent('mousedown', clientCoordinatesForScreenPosition([10, 0]), button: 1))
+        componentNode.querySelector('.scroll-view').dispatchEvent(buildMouseEvent('mouseup', clientCoordinatesForScreenPosition([10, 0]), which: 2))
+        expect(atom.clipboard.read()).toBe 'sort'
+        expect(editor.lineTextForBufferRow(10)).toBe 'sort'
 
   buildMouseEvent = (type, properties...) ->
     properties = extend({bubbles: true, cancelable: true}, properties...)
diff --git a/src/text-editor-component.coffee b/src/text-editor-component.coffee
index 51c4447b6..743e44778 100644
--- a/src/text-editor-component.coffee
+++ b/src/text-editor-component.coffee
@@ -404,7 +404,7 @@ TextEditorComponent = React.createClass
     window.addEventListener 'resize', @requestHeightAndWidthMeasurement
 
     @listenForIMEEvents()
-    @listenForMiddleMousePaste() if process.platform is 'linux'
+    @trackSelectionClipboard() if process.platform is 'linux'
 
   listenForIMEEvents: ->
     node = @getDOMNode()
@@ -432,21 +432,21 @@ TextEditorComponent = React.createClass
       editor.insertText(selectedText, select: true, undo: 'skip')
       event.target.value = ''
 
-  listenForMiddleMousePaste: ->
-    clipboard = require 'clipboard'
-
-    @refs.scrollView.getDOMNode().addEventListener 'mouseup', ({which}) =>
-      return unless which is 2
-
-      if selection = clipboard.readText('selection')
-        @props.editor.insertText(selection)
-
-    @subscribe @props.editor.onDidChangeSelectionRange =>
-      if selectedText = @props.editor.getSelectedText()
+  # Listen for selection changes and store the currently selected text
+  # in the selection clipboard. This is only applicable on Linux.
+  trackSelectionClipboard: ->
+    timeoutId = null
+    {editor} = @props
+    writeSelectedTextToSelectionClipboard = =>
+      return if editor.isDestroyed()
+      if selectedText = editor.getSelectedText()
         # This uses ipc.send instead of clipboard.writeText because
         # clipboard.writeText is a sync ipc call on Linux and that
         # will slow down selections.
         ipc.send('write-text-to-selection-clipboard', selectedText)
+    @subscribe editor.onDidChangeSelectionRange ->
+      clearTimeout(timeoutId)
+      timeoutId = setTimeout(writeSelectedTextToSelectionClipboard)
 
   observeConfig: ->
     @subscribe atom.config.observe 'editor.useHardwareAcceleration', @setUseHardwareAcceleration
@@ -560,7 +560,11 @@ TextEditorComponent = React.createClass
       scrollViewNode.scrollLeft = 0
 
   onMouseDown: (event) ->
-    return unless event.button is 0 # only handle the left mouse button
+    unless event.button is 0 or (event.button is 1 and process.platform is 'linux')
+      # Only handle mouse down events for left mouse button on all platforms
+      # and middle mouse button on Linux since it pastes the selection clipboard
+      return
+
     return if event.target?.classList.contains('horizontal-scrollbar')
 
     {editor} = @props
@@ -769,15 +773,21 @@ TextEditorComponent = React.createClass
       # Stop dragging when cursor enters dev tools because we can't detect mouseup
       onMouseUp() if event.which is 0
 
-    onMouseUp = ->
+    onMouseUp = (event) ->
       stopDragging()
       editor.finalizeSelections()
+      pasteSelectionClipboard(event)
 
     stopDragging = ->
       dragging = false
       window.removeEventListener('mousemove', onMouseMove)
       window.removeEventListener('mouseup', onMouseUp)
 
+    pasteSelectionClipboard = (event) ->
+      if event?.which is 2 and process.platform is 'linux'
+        if selection = require('clipboard').readText('selection')
+          editor.insertText(selection)
+
     window.addEventListener('mousemove', onMouseMove)
     window.addEventListener('mouseup', onMouseUp)