It's a really good question...
I started on an HP700, it created the .emacs file and I was always confused about what I had written myself and what emacs was doing. Then I started on an Sun Workstation and there they had installed XEmacs. It was there where i stumbled across the .emacs.d/custom.el file and I found the idea cool. I investigated a bit and adopted loading the custom file. <mea culpa>I never investigated how customisation where added to .emacs </mea culpa>
I don't know how common my way of working is but I try out things using Custom and then, if I adopt them, they become a part of my permanent config.
Maybe Custom wlll need to check and eventually remove customisations from .emacs if custom-file is defined... would that be feasible? IT isn't something you do 10 times a second, right?
Best, /PA