It really depends on the type of Chamois Cream you are using. I use Assos and that has a little bit thicker consistency than Vaseline, so it typically takes a bit more to get a good spread across everything.
The rule of thumb I follow is anywhere where friction will be a factor. That for me means most of the taint, and the inner part of the upper thigh. I don't like applying it to padding in the bib because I hate that feeling when I first put it on (worse than a wet bathing suit). I know of some riders, such as my dad, who will also apply a fresh coat after being on the bike for a couple of hours.
After applying I try to wash my hands (when a sink is handy), when it is not then I use one of the handi-wipes I keep in my saddle bag.
I agree with @Daniel, there really isn't a wrong way to do it. I would try out different ways on shorter rides to see what feels good and what does not.