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Remember that the Design View is not a WYSIWYG browser.You can get closer with Live View, but that's not a browser either.
If you have designated areas as editable regions on your Template and have Invisible Elements showing ... like the blue tab at the top of each editable region...alignment of your divs will APPEAR to be displaced. Those blue tabs DO take up a little bit of real estate, you know! Turn off the Invisible Elements, and your layout will "snap" back into place.
Why do you think a div cannot be designated as an editable region? You can either include the whole div, tags and all...in which case the tags will become editable...or include just the contents of the div, which will protect the div tag from harm. Same with a heading tag. You just have to be careful of your nesting, and not include the open tag in the editable region if you have not also included the closing tag.
You can also designate attributes of tags as editable.
If you have created a Template and indicated when you saved it as a Template that you wanted pages updated when the Template changes (one of the more obvious reasons for using a Template, by the way), yes, changes to the Template will propagate to the child pages made from that Template. The only parts that will change on the child page, though, will be in the ineditable regions.
The deal with a Template is that it is not, strictly speaking, a PAGE, it is a Template for creating pages. Two different beasts altogether. LIke the difference between a cookie cutter and a cookie. They may both be the same shape, but only one of them is a cookie.
I think you would enjoy running through some of the tutorials here on the Adobe site. They will give you additional insight into the workings of Dreamweaver CS4. The tutorials and the Adobe TV videos are well worth the time you take to do and view them.
http://www.adobe.com/devnet/dreamweaver/ for the tutorials page.
http://tv.adobe.com/ for Adobe TV.