I had to raise the limit in /usr/local/hestia/php/etc/php-fpm.conf
[global]
rlimit_files=65535
See PHP: Configuration - Manual
Then systemctl restart hestia and everything is working.
The default as detected with prlimit --pid= was 1024, I would suggest adjusting that up by default. This took me many hours of work to debug and fix for good.
Can I somehow make this change permanent? Hestia will probably overwrite it on upgrade…