As always, these are generic guidelines — depending on where you’re applying and what your committee says, you might need to tweak these suggestions.
Keep your job letter short — 2 pages, 12 point font, single-spaced. You’ll want to include much more, but the goal is to get an invitation for a campus visit. So, to get there, give your reader some interesting things to think about, index that you’re a potentially interesting colleague, and leave them wanting more — if you tell them too much, you run the risk of people feeling like they already know all there is to know about you…
The form is pretty generic:
1) Address the job you’re applying for and give a sense of your interests & training
2) Give a 1 paragraph summary of your dissertation
3) Give a 1 paragraph summary of your next project and how it relates to your dissertation
4) Write about your teaching interests & pedagogy in 1 paragraph
5) Write about your broad research interests in 1 paragraph
6) Close by addressing possible synergies between you and the department you’re applying to — show that you know something about the faculty as potential colleagues, but don’t overdo it.
The best job letters are anxiety-free. That might seem difficult, but if you write about what you know and your strengths, that will help to minimize any textual stress…
You can see a copy of my sample job letter with commentary here:
Matthew Wolf-Meyer 
Hi, historian here. Your advice is helpful and I’d like to add to it. I teach at a small state university with a 12-credit teaching load. When hiring, I very frequently see cover letters that would be perfect for R1 jobs but are surprisingly wide of the mark for our institution. I can see that candidates have been coached “wrong” for our kind of school in many other ways too. With two colleagues at similar schools who’ve had parallel observations, I’m giving a workshop about this at the Organization of American Historians conference in April 2019. We wrote a blog piece about our thoughts here: https://www.oah.org/insights/posts/2019/1/applying-for-jobs-at-teaching-institutions-or-so-what-else-can-you-teach/
Hi Rebecca — this is great, thanks for sending it along. If you have an update after the meetings, please do send along the link!