Because the example sample is very simple (the preview rect is in the top right corner of the window), it's actually just a bit more complicated than what I though, but I think I've mosty found a good workaround:

- I run all my handles code twice (just the parts calling stuff like Handles.PositionHandle) (except during Repaint events where I only call it once so that it doesn't get drawn twice)

- With all the previous code untouched (including the calculations on lastRepaintCameraRect), on the first call I set my cursor position this way:
Vector2 newMousePosition = baseMousePosition + new Vector2(-lastRepaintCameraRect.x, lastRepaintCameraRect.y + lastRepaintCameraRect.height - position.height);
newMousePosition.y -= 22f;
Event.current.mousePosition = newMousePosition;

And for the second call:
newMousePosition = baseMousePosition + new Vector2(-lastRepaintCameraRect.x, lastRepaintCameraRect.y);
newMousePosition.y -= 22f;
Event.current.mousePosition = newMousePosition;

It does have several downsides though (the handle doesn't feedback the use of the arrows tips, and I also have invisible flying handles at various offsets from the visible ones).

After further investigation, it looks like the plane handles and arrows body (not the tip) respond correctly when only offsetting the Event.current.mousePosition by the window's header height.
So as far as I understand it, in the previous versions, all parts of the handles respond to the mouse position being offsetted as it is in the provided code; but in the earlier versions, only the arrows tips still need that offset, and all other parts of the handle now respond to the normal cursor position with a slight offset.

This code works for the arrows tips:
Vector2 newMousePosition = Event.current.mousePosition + new Vector2(-lastRepaintCameraRect.x, lastRepaintCameraRect.y);
newMousePosition.y -= 22f; // Empirical height of the window
Event.current.mousePosition = newMousePosition;

And for the rest of the handle:
newMousePosition = Event.current.mousePosition;
newMousePosition.y -= 22f; // Empirical height of the window
Event.current.mousePosition = newMousePosition;

Please note that the squares at the root of the arrows (to move the handle along a plane) aren't registering the cursor at all either.