Description
Dragging files onto a file upload region doesn't work on Linux, it is upstream CEF Issue #1418. On Windows dragging files do work fine, tested with CEF v55. From the referenced CEF issue you can conclude that it should also work fine on Mac. So it seems that this is Linux only issue. It was reported about two years ago and still not fixed, so it seems to have low priority. Make a vote for it on bitbucket if you need it.
Testing this example: https://css-tricks.com/examples/DragAndDropFileUploading/
Reported Linux problem on the CEF Forum: http://magpcss.org/ceforum/viewtopic.php?f=6&t=14738
Temporary fix
I think you could make it work in your app on Linux by using e.g. wxPython drag&drop API to handle files being dropped onto CEF control. Then you would use javascript bindings or XHR request handled through RequestHandler callbacks, to transfer the contents of the file being dropped to javascript. XHR request would be more performant for big files. This is all assuming you have control over javascript code running in CEF browser.