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I run everything on one droplet. It's less overhead for me and also cheaper, since most of the stuff I host has very little resource requirements.
#givewithella runs on a DO droplet with s3 for assets
Small NodeJS stuff runs on the same droplet, while more extensive stuff needs a dedicated one, so it doesn't compete for resources. I do NodeJS almost exclusively, and you can easily manage Node apps with PM2, etc.
I mean, it's not really advisable to run some mission critical stuff on the same droplet as everything else. If shit hits the fan, you better have hourly backups at hand.
The projects I've migrated from Heroku to Linode are all on the same server for now. My plan is to spin them off to their own server once they generate enough revenue and require enough resources to warrant the cost increase.
As @matthewmorek points out there is some risk involved in having everything in one server. The way I see it all the risk of the independent apps are added together. If one breaks or gets hacked, etc, it might bring everything else down with it. So roughly speaking a server with 10 sites is 10 times as likely to fail. Then again it might also be 10 times as easy to manage. (e.g. no need to upgrade the OS or critical updates in 10 different places).
Disclaimer: I have very little VPS experience. I've been using Heroku forever and only recently started looking into VPS-based hosting seriously.