-First, on a template, will WordPress automatically put main content in a div called "content"?
Technically, your template will do that, or it won't do that. It has everything to do with your template and not much to do with wordpress itself.
If you don't want that to happen you are free to adjust your template so it doesn't happen.
what if i want multiple content divs on a single page? Much like the wordpress.org home page. Is it possible to have multiple editable content sections on a single page which can be edited through wordpress? If so, how would I set up the html? Do i need to give the divs special id's or something?
It is, but it has very little to do with the HTML - do what you want with the HTML.
A template extracts content from the database into the HTML of your choosing - so basically, make the HTML what you want it - then stick the content where you want it to be, with Template Tags and one The Loop (tm), or multiple loops... or any number of other ways to stuff your HTML full of editable content.
-I noticed that some themes are "widget-ready" what does that mean? What has to be done to a template to make it "widget-ready"
Widgets are sidebar toys - they make it easy for people scared to edit their PHP files to use certain plugins and reorder their sidebar. Basically widgets are pointless for someone planning to write their own custom theme for use as a CMS.
... unless you intend to package that template for download/use by non-technical folks.