diff --git a/autoload/youcompleteme.vim b/autoload/youcompleteme.vim
index e89cdfe5fa..31321a3715 100644
--- a/autoload/youcompleteme.vim
+++ b/autoload/youcompleteme.vim
@@ -475,7 +475,9 @@ function! s:SetUpCompleteopt()
   " Also, having this option set breaks the plugin.
   set completeopt-=longest
 
-  if g:ycm_add_preview_to_completeopt
+  if g:ycm_add_preview_to_completeopt ==# 'popup' && exists( '*popup_open' )
+    set completeopt+=popup
+  elseif g:ycm_add_preview_to_completeopt
     set completeopt+=preview
   endif
 endfunction
diff --git a/python/ycm/client/completion_request.py b/python/ycm/client/completion_request.py
index 50e53ec443..16293ccd7e 100644
--- a/python/ycm/client/completion_request.py
+++ b/python/ycm/client/completion_request.py
@@ -181,11 +181,25 @@ def _GetCompletionInfoField( completion_data ):
 
 def _ConvertCompletionDataToVimData( completion_data ):
   # See :h complete-items for a description of the dictionary fields.
+  extra_menu_info = completion_data.get( 'extra_menu_info', '' )
+  preview_info = _GetCompletionInfoField( completion_data )
+
+  # When we are using a popup for the preview_info, it needs to fit on the
+  # screen alongside the extra_menu_info. Let's use some heuristics.  If the
+  # length of the extra_menu_info is more than, say 50% of screen, truncate it
+  # and stick it in the preview_info.
+  if vimsupport.UsingPreviewPopup():
+    max_width = max( int( vimsupport.DisplayWidth() / 3 ), 3 )
+    extra_menu_info_width = vimsupport.DisplayWidthOfString( extra_menu_info )
+    if extra_menu_info_width > max_width:
+      preview_info = extra_menu_info + '\n\n' + preview_info
+      extra_menu_info = extra_menu_info[ : ( max_width - 3 ) ] + '...'
+
   return {
     'word'     : completion_data[ 'insertion_text' ],
     'abbr'     : completion_data.get( 'menu_text', '' ),
-    'menu'     : completion_data.get( 'extra_menu_info', '' ),
-    'info'     : _GetCompletionInfoField( completion_data ),
+    'menu'     : extra_menu_info,
+    'info'     : preview_info,
     'kind'     : ToUnicode( completion_data.get( 'kind', '' ) )[ :1 ].lower(),
     # Disable Vim filtering.
     'equal'    : 1,
diff --git a/python/ycm/vimsupport.py b/python/ycm/vimsupport.py
index 93d5b676b3..292d4db712 100644
--- a/python/ycm/vimsupport.py
+++ b/python/ycm/vimsupport.py
@@ -1304,3 +1304,15 @@ def ScreenPositionForLineColumnInWindow( window, line, column ):
       WinIDForWindow( window ),
       line,
       column ) )
+
+
+def UsingPreviewPopup():
+  return 'popup' in ToUnicode( vim.options[ 'completeopt' ] ).split( ',' )
+
+
+def DisplayWidth():
+  return GetIntValue( '&columns' )
+
+
+def DisplayWidthOfString( s ):
+  return GetIntValue( "strdisplaywidth( '{}' )".format( EscapeForVim( s ) ) )