2015 update: the flexbox approach

There are two other answers briefly mentioning flexbox; however, that was more than two years ago, and they don't provide any examples. The specification for flexbox has definitely settled now.

Note: Though CSS Flexible Boxes Layout specification is at the Candidate Recommendation stage, not all browsers have implemented it. WebKit implementation must be prefixed with -webkit-; Internet Explorer implements an old version of the spec, prefixed with -ms-; Opera 12.10 implements the latest version of the spec, unprefixed. See the compatibility table on each property for an up-to-date compatibility status.

(taken from https://developer.mozilla.org/en-US/docs/Web/Guide/CSS/Flexible_boxes)

All major browsers and IE11+ support Flexbox. For IE 10 or older, you can use the FlexieJS shim.

To check current support you can also see here: http://caniuse.com/#feat=flexbox

Working example

With flexbox you can easily switch between any of your rows or columns either having fixed dimensions, content-sized dimensions or remaining-space dimensions. In my example I have set the header to snap to its content (as per the OPs question), I've added a footer to show how to add a fixed-height region and then set the content area to fill up the remaining space.

html,
body {
  height: 100%;
  margin: 0;
}

.box {
  display: flex;
  flex-flow: column;
  height: 100%;
}

.box .row {
  border: 1px dotted grey;
}

.box .row.header {
  flex: 0 1 auto;
  /* The above is shorthand for:
  flex-grow: 0,
  flex-shrink: 1,
  flex-basis: auto
  */
}

.box .row.content {
  flex: 1 1 auto;
}

.box .row.footer {
  flex: 0 1 40px;
}

<!-- Obviously, you could use HTML5 tags like `header`, `footer` and `section` -->

<div class="box">
  <div class="row header">
    <p><b>header</b>
      <br />
      <br />(sized to content)</p>
  </div>
  <div class="row content">
    <p>
      <b>content</b>
      (fills remaining space)
    </p>
  </div>
  <div class="row footer">
    <p><b>footer</b> (fixed height)</p>
  </div>
</div>

In the CSS above, the flex property shorthands the flex-grow, flex-shrink, and flex-basis properties to establish the flexibility of the flex items. Mozilla has a good introduction to the flexible boxes model.

This can now be done in Chrome, Safari, Firefox 4+, and Internet Explorer 10pp4+!

See this question's answer for more information: Updating address bar with new URL without hash or reloading the page

Example:

 function processAjaxData(response, urlPath){
     document.getElementById("content").innerHTML = response.html;
     document.title = response.pageTitle;
     window.history.pushState({"html":response.html,"pageTitle":response.pageTitle},"", urlPath);
 }

You can then use window.onpopstate to detect the back/forward button navigation:

window.onpopstate = function(e){
    if(e.state){
        document.getElementById("content").innerHTML = e.state.html;
        document.title = e.state.pageTitle;
    }
};

For a more in-depth look at manipulating browser history, see this MDN article.