overflow:
The behavior of the 'auto' value is user agent-dependent, but should cause a scrolling mechanism to be provided for overflowing boxes.
As such, they are free to provide the scrollbar wether it's needed or not, in the same way as it's required with overflow: scroll. And if you change it to overflow: scroll, the right side image is moved down in the exact same way in other browsers as well (checked FF3).
So, either overflow: hidden, or increase width of #wrapper_content_directory to 883px (and change how you apply the background colour or it won't look nice in browsers that don't show the scrollbar), or both change width and set overflow: scroll.
And if you do change the width, do double check the value I suggested in all browsers reelvant to you. I'm uncertain if SB widths differ between browsers, but iirc IE8, Safari 4 and FF3 all have 15 or 16px scroll bars.