I spun up Wireshark and looked at the SMB traffic right before the crash. From there it became obvious that the issue was caused by me serving the files from a Samba share backed by a TMSU fuse VFS. Specifically it is caused by this somewhat non-standard TMSU behavior, which also caused similar problems in MPC-HC.
In the specific case of Heresphere, the crash is caused by Heresphere attempting to open .hsp, .ass, .ssa, and .srt files with the same basename as the video. This will result in TMSU serving the actual video file under these alternate names, which causes Heresphere to crash as it's basically reading garbage.
Since TMSU is a very niche piece of software I doubt anyone else will come across this, but regardless, for robustness I think it would be a good idea for Heresphere to ignore garbage .hsp/.ass/.ssa/.srt (without attempting to read them till the end) instead of crashing.
For those who are actually serving from a TMSU-backed Samba share, the following smb.conf config will work around the issue:
veto files = *.hsp/*.ass/*.ssa/*.srt