After Updating puppet server from 3.8.7 to 4.10 on Foreman 1.15.1.
I am getting the same error messages as you did on client machines, 'Error: 
Could not retrieve catalog from remote server: Error 500 on SERVER...'

I 
followed 
http://projects.theforeman.org/projects/foreman/wiki/Upgrading_from_Puppet_3_to_4

My puppet.conf has vardir = /opt/puppetlabs/puppet/cache

And I copied /var/lib/puppet/foreman_cache_data to 
/opt/puppetlabs/puppet/cache/foreman_cache_data

You said, 'I fixed this by setting the correct puppet cache directory for 
foreman'. Can you please let me know what exactly you did?

Thanks

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