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COMPANY HIRING GUIDE

How to apply to Handshake

What Handshake is hiring for and what its application asks, from the postings and application forms we checked. Newest posting added 2026-10-02.

  • 78 open roles across 40 job titles
  • 28 new open roles in the last 30 days
  • Applications on Ashby
  • Locations: San Francisco, US; Remote · San Francisco, US; Bengaluru, IN; Seattle, US; New York, US; Nashville, US; Remote · Trust And Safety, US; San Francisco, CA, CA

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Tailor your resume to a Handshake job, free

Remote roles at Handshake

15 openings open to remote applicants in the US.

Handshake Ashby careers site and sign-in

Handshake posts the jobs listed here on Ashby, its applicant tracking system, at jobs.ashbyhq.com. To apply, open a posting below and follow its link to apply on Handshake’s site. If that site asks you to sign in, use or create an account there: it is separate from your Applystead account.

Tailor your resume to a Handshake posting free

About Handshake

Which applicant tracking system does Handshake use?

The Handshake postings listed here are hosted on Ashby (79 open postings), where you apply.

Hiring signals

  • Pay transparency: 15% of open postings list pay set by the employer (12 of 79 postings)
  • Postings list updated:

Open roles at Handshake

Other openings at Handshake

Handshake hiring process: how to apply

From the Handshake postings listed here and 1 application form we checked.

  1. Choose a role above and open its posting.
  2. Apply on Handshake’s Ashby application page (how to apply on Ashby).
  3. Fill in the form: it asks for contact details, resume or CV, cover letter, voluntary self-identification (EEO), plus about 2 questions specific to Handshake.

What the Handshake application asks

From 1 application form we checked (2026-10-06). Only the kinds we saw asked are listed.

QuestionAsked on
Resume or CVat least 1 of 1 form we checked
Cover letterat least 1 of 1 form we checked
Voluntary self-identification (EEO)at least 1 of 1 form we checked

Questions only Handshake asks

  1. How did you hear about this job? asked on 1 of 1 form
  2. Name Pronunciation asked on 1 of 1 form

See Handshake salaries

Employers in the same industry as Handshake or on the same application system, hiring now.

Prepare your Handshake application

Free tools for your Handshake application

Guides

Questions about applying

What ATS does Handshake use?

The Handshake postings listed here are hosted on Ashby (79 open postings), where you apply. Handshake has 78 open roles listed here.

Is Handshake hiring right now?

Yes. Handshake has 78 open roles listed as of 2026-10-06.

What does the Handshake application ask?

The 1 application form we checked ask for contact details, resume or CV, cover letter and voluntary self-identification (EEO). Questions only Handshake asks include “How did you hear about this job?” and “Name Pronunciation”.

Does Handshake ask for a cover letter?

Yes. At least 1 of the 1 Handshake application form we checked asks for a cover letter.

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