You'll probably want to run it on the LTM. If you need SSL you can configure SNI - that'll allow you to use a single IP-address for multiple hostnames. With the demise of Windows XP there aren't many clients that are not compatible with SNI.
If you have a lot of hostname you should consider using a data class (group) with key/value pairs for the hostnames and the pool names (or even nodes).
Also, since it sounds like you're consolidating, have you considered hosting multiple hostnames under a single web server instance? For some of the smaller sites I have provisioned I use an iRule that re-writes the URI to a specific folder on a web instance. The folder names match the hostnames, which allows our editors to simply create a new site by creating a folder that equals the hostname. After configuring the DNS the site is live. Since we're using a file server and multiple web servers there's also redundancy.