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You will need a reverse Proxy that can handle name-based virtual hosts, one for each domain (each with its own certificate). nginx would be one candidate for that.
+1 for nginx, although there has been some concern because nginx is developed by a group of russians though it is open source and appears to still be widely used. If this worries you, look into traefik.
Otherwise does your ProxMox setup run docker containers? If so you can use NginxProxyManager which has a web gui for configuring your virtual hosts.
At a high level what you need is this:
Tl;dr: you can add millions of sites to a single IP if you want. Very common in commercial hosting as well.
I would advise against running millions of domains on a single IP, you will run into issues with a lack of ports that are not in use for the reverse proxy/backend connections unless you are dealing with websites that are basically never used.
Sure.. this was just said to simplify what is technically possible. Should you? No maybe not, for multiple reasons. Can you, technically? Yes absolutely. I don't know what's the limit but I know that if you have to ask here on lemmy, you might not be anywhere near that limit. Unless you are the go daddy.
I mean... if you're running millions of sites on one box, and that itself isn't an issue, I'd assume your port saturation/traffic is pretty low.
Sweet sounds like I've got some reading to do, thanks!