I started exploring the idea of custom drawing functions to simplify the list header, and maybe get around the problem. I created a project consisting of the example code for the CanvasItem custom drawing tutorial. Even this project exhibits the vertical flickering problem.
This made me wonder what the simplest way of reproducing the problem was. So I created an even simpler minimal project to reproduce the error: A single label (text: "Watch me flicker!", everything else left to default values) in the middle of the window. It's so simple, you can probably create it yourself faster than it would take you to download, decompress, import and run it. I put the label in the middle of the window (by dragging with the mouse) so the full effect of the problem can be easily seen: The label gets drawn above and below the correct location, depending on whether the window height is increasing or decreasing, but never off to the side.
Interestingly, the new bug demo project shows the problem in 3.2.1-stable, but not in the 4.0/master branch.
So this problem might already be fixed in the 4.0/master branch. I just tried reproducing it with both the new demo project and just the editor window, and it resizes fairly smoothly the way it should. There is still a bit of update lag on the right and bottom edges when the window is being resized quickly, but not nearly as bad as with 3.2.1-stable.