I dealt with this for a couple of days, but it finally got on my nerves so I decided to find the issue and fix it.
It turned out to be a simple fix. The version attribute in the .flexLibProperties file was set to 1.
I guess when converting these flex lib projects from Flex Builder 3 to Flash Builder 4, the version never got updated. In Flash Builder 4, the version number should be set to 3.
Updating the version attribute to 3 fixed the issue. The include all classes from all source paths worked now between closing and opening Eclipse.