At most places where I've seen this done, the candidate is asked to present something from hir research or creative activity. Sometimes, I know search committees ask for something special, a sort of please introduce us to this specific issue or whatever.
From a candidate's perspective, the research/creative activity talk makes so much more sense, especially if you've got a couple of campus visits, because you can basically give the same talk at each of the visits, and you'll have time to focus on it and really polish it.
The other seems like hell, and I'd argue against it were I on the committee. (It's worth knowing, perhaps, that the committee doesn't always communicate such requests to the department at large before the candidate does the talk. Alas, we aren't always great communicators.)
I went to a job talk recently, and was at least as interested in watching my colleagues' responses as I was in what the candidate had to say. Some colleagues were all nods, and afterwards very happy, others were clearly uncomfortable, and afterwards not so happy. The happy ones are fine. It's the ones who were uncomfortable that probably say something about what people are looking for, at least in a department such as my own (a regional comprehensive).
Let me use my old standby, underwater basketweaving. The candidate was
talking about the effect of salinity levels on the meanings of deep
water basket weave tightness. The happy, nodding people were in basically a related field, pretty much. So when the candidate talked about salinity levels, they were thinking about the methodology of measuring salinity levels and the effects on reed pliability, and how the material affects the meaning and how they teach students to manage weave tightness.
The uncomfortable people were uncomfortable for a variety of reasons. And it's worth recognizing that some people are more willing to be uncomfortable, or, as we say in basketweaving circles, out of their depth. And some really hate it.
J was uncomfortable because J is a deepwater weaver, and J has very strong opinions about weaving, and doesn't really believe that salinity levels affect meaning at all.
C was uncomfortable because C is in historical basketweaving and wants to hear about the historical changes in salinity levels; modern salinity measurements just don't cut it for C, you know.
Then what's a candidate to do?
As I listened to J and C, and realized that my own interests were sparked by some of the talk, but that I thought C's desire for a greater historical understanding ("Always historicize.") was partly mine, too.
But a candidate can't know that. And let's face it, the candidate's work is what it is.
But, and I think this is most important, a candidate can make sure that they're talking in a way that won't limit their audience just to people who do exactly what they do.
I think of it like this, I suppose:
When you're first in grad school, you spend a whole lot of time trying to sound smart, adopting the language of your field, trying to understand it fully. You read Jameson, and then start quoting him as if of course, everyone should just know that.
The height of this comes when you're in the depths of your dissertation. You think of everything in terms of your dissertation, perhaps, or at least a lot. You're self-absorbed. And since most of your grad school cohort is also writing, you have lots of conversations about very theoretical issues, history, critics, sources, and so on. You speak your own language. And sometimes you forget that others don't speak that language. Or maybe they just don't care.
And then you start teaching the stuff you've been working on, and you realize that you need to talk differently to communicate to undergraduates.
And then you keep teaching, and you realize that sometimes the most difficult issues need to be communicated more effectively, that people who do physics want to understand what you do, but they don't have time to read De Certeau because they're working hard on their own stuff. But they're smart. And you ask them physics questions, and you learn that they can explain really complicated physics stuff so that you can understand, even if you can't do the calculus in your head. And then you learn to communicate with the physics folks, and the anthro folks, and your students and your peers at conferences. Or maybe you never quite get there, but you can see others do it, and know it's worth doing.
Maybe, as one of my colleagues said, you realize that something else is really important to you, and you aim everything at communicating that, and you realize that you care more about speaking to a different audience than to other salinity theorists.
So for the successful job talk, you need to get beyond talking to other dissertators, and get to talking to people who aren't salinity experts, to people who don't speak the exact language of your dissertation, and to help them see why your research work matters and why they should care anyway.