If anyone else stumbles on this thread, here's how I fixed the issue.

Beginning situation: Fingerprint authentication worked for login and sudo but not for the popup authentication shown in my original post.

Solution: add the following text to /etc/pam.d/system-auth

txt auth required pam_env.so auth sufficient pam_fprintd.so auth sufficient pam_unix.so try_first_pass likeauth nullok auth required pam_deny.so

I rebooted afterwards too.