Ok, let me see if I'm interpreting correctly:
In the first run, the one with small window, you used scroll wheel or keyboard arrow and they did two things - it scrolled the contents of the list but also started selecting object in "File" box.
In second run, you made the window bigger, but did not seem to use scroll wheel or keyboard arrows so the File box did not change.
What you would like to have essentially is that using scroll wheel / keyboard arrows only scrolls the list up and down but does not select anything, correct? If so, it this how Requesters work on AmigaOS?