This is my first time in the job market in over 15 years. I'm a little at a loss on how to find or apply for a job. How long are cover letters supposed to be these days?

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Depending on where you are applying, and the level of the role, may determine whether the cover letter is needed at all. With a deluge of resumes these days, we don’t review cover letters. Hiring manager “might”, but it is not used as a determinant for interview preference. The exception may be, senior level management roles. The manager is more likely to review the cover letter. 1-Page should do the trick, and I’d recommend you connect the dots for the audience. Why you are a fit for THIS role. Which also would require customization. The juice may not be worth the squeeze, unless you are applying to a finite amount of positions.

I say that to say, it may be a fruitless effort. Getting an offer these days depends on LUCK, and/or referrals from an employee.

Cover letters are optional. It should be not more than 300-400 words.
There are several staffing companies, where you can register yourself.

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