OK after more research, I discovered that what I'm looking for is called a dot leader. While the W3C Working Draft has a section on them here, they don't seem to be well-implemented yet. I found another approach on SO here. Using that answer, I revised my code as follows:
HTML:
<header>
<h1>Title</h1>
<span>Category</span>
</header>
CSS:
header {
overflow: hidden;
}
h1 {
float: left;
padding: 0 .4em 0 0;
margin: 0;
}
span {
float: right;
padding: 0 0 0 .4em;
margin: 0;
}
/* Dot Leader */
header:after {
content: "";
display: block;
overflow: hidden;
height: 1em;
border-bottom: 1px dotted;
}
Here's a JSFiddle with the result: http://jsfiddle.net/dx48R/