Answer: Every one you are qualified for.
Ms. PhD. has a post up right now in which she mentions her job application strategy.
A well-meaning former colleague sent me an ad for a faculty position in another city, at a school where I don't know anyone.
I said thank you. What's the point in explaining that I'm not going to waste my time and energy applying? I took it as a compliment that she seems to think I deserve a faculty position.
In the comments section, she answers PiT's question about the above statement with:
Well, it's possible that I don't know anyone there because they're not famous. But the practical issue is that it's nearly impossible to get an interview if you don't know anyone at the school, and in the long run, you'll never get any useful feedback if for some reason you have an interview but don't get the job. That's what happened to me last time. I got some bullshit explanation, which I couldn't (can't) address in future applications....
....So far as I can tell, there is no point in going through the stress and heartbreak again when the economy is only getting worse, especially in academia. I've literally seen maybe less than 10% of the ads there were last year, and last year was down to maybe 20% of the ads I had seen in previous years.
I don't think applying blindly to ads works in my field. You absolutely have to know people, preferably multiple people in the same department, who will ACT on your behalf. The departments are too big, and there are factions within them. Even if half the department wants you, if the other half wants someone else, you're very likely screwed.
Okay then. We'll assume that Ms. PhD. is right about her field and that it's not worth applying to a university unless you have someone pulling for you. I would suggest, however, that this is not the case for most fields (Ms. PhD did not claim it was, BTW, nor did she offer the above as advice to others, simply stated her situation). I didn't know anyone in the department that hired me, aside from being 'conference familiar*' with one individual.
I have had several postdocs I know ask me about applying for certain jobs and my advice is the same: send it in! If you don't apply, you are certain to not get the position. Worry about whether it is the perfect place for you after you have interviewed and after you have an offer. When I interviewed for jobs I would say that I was pleasantly surprised by one I thought would not be a good fit and came away with more questions than I expected from one I thought was perfect. But I never would have had that insight without applying.
Have two or three different application packets ready that you can send to the different types of jobs you qualify for and get them out there. If you have them already done up, the effort per application is not particularly high. Don't spam the world, but you should be able to find at least 10 positions a year (and many more in a good year) that you could fit into.
Don't assume you know anything about a department, university, city or part of the country without checking it out. The worst case scenario is that your suspicions are confirmed and you decline an offer. So what? You still had some interview experience and got your name out there.
I also often hear people say that they don't want to bother their letter of reference writers if they are not completely serious about a job. You know what, you LOR writers expect you are going to apply to a lot of places and, I hate to tell you, but they are just changing the address on the top and sending it off. You can pay than back when you have a job.
In the fields I am familiar with (and I'm sure there is lots of variation out there), either you are serious about finding a job and you get your apps out there or you are not. If you are not and you only send your application to a select few places, then you better have a back-up plan because you are stacking the odds against you. It also means that your first interview might be at your dream spot, and it's a good idea to have a little experience with the two day marathon you have to go through so you can have your routine down before you get to the one you really want.
Now go scour those listings and make yourself fit the descriptions. You and the committee might be pleasantly surprised by your interview.
*As in, talked to them briefly once at one conference and maybe saw them across the room at another.