Navigate->File fails to find existing files Follow

My project has several content roots, many of which have paths with the same names (for example content roots A and B, both have path x/y/z). Navigate->File fails to find many files that do exist on some content root. The content roots also have symlinks to some of its sub folders.

I enabled #com.intellij.util:trace in the Custom Debug Log Configuration, and that seems to show the indexing never going down certain paths, but maybe logs are rolling over before I can catch it. 

I tried to reproduce this with a separate project, but couldn't :-/

Any suggestion of how fix or further debug this?

A few days ago I created https://youtrack.jetbrains.com/issue/PY-35570 but maybe a community post is a better option.