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.
There are a couple of CSS 3 measurement units called:
What are Viewport-Percentage Lengths?
From the linked W3 Candidate Recommendation above:
The viewport-percentage lengths are relative to the size of the initial containing block. When the height or width of the initial containing block is changed, they are scaled accordingly.
These units are vh (viewport height), vw (viewport width), vmin (viewport minimum length) and vmax (viewport maximum length).
How can this be used to make a divider fill the height of the browser?
For this question, we can make use of vh: 1vh is equal to 1% of the viewport's height. That is to say, 100vh is equal to the height of the browser window, regardless of where the element is situated in the DOM tree:
HTML
<div></div>
CSS
div {
height: 100vh;
}
This is literally all that's needed. Here is a JSFiddle example of this in use.
What browsers support these new units?
This is currently supported on all up-to-date major browsers apart from Opera Mini. Check out Can I use... for further support.
How can this be used with multiple columns?
In the case of the question at hand, featuring a left and a right divider, here is a JSFiddle example showing a two-column layout involving both vh and vw.
How is 100vh different from 100%?
Take this layout for example:
<body style="height: 100%">
<div style="height: 200px">
<p style="height: 100%; display: block;">Hello, world!</p>
</div>
</body>
The p tag here is set to 100% height, but because its containing div has 200 pixels height, 100% of 200 pixels becomes 200 pixels, not 100% of the body height. Using 100vh instead means that the p tag will be 100% height of the body regardless of the div height. Take a look at this accompanying JSFiddle to easily see the difference!
Best Answer
It looks like the conventional method of simply adding the extra height still works, but now it seems the value to add is 69px instead of 60px.