Public Sector Account Director

handshakeΒ· Employer Revenue
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🌍 RemoteπŸ“ Remote (USA)FullTimeπŸ’° USD 260K–300K/yr

About this role

About Handshake

Handshake was founded on a simple belief that everyone deserves a path to a great career, regardless of where they went to school or who they know. Today, we power 25 million job seekers, 1 million+ employers, and 1,600 educational institutions.

In 2025, we started Handshake AI and built the fastest-growing AI data business in history. We work directly with frontier AI lab researchers to create evaluations, publish benchmarks, and push the boundary of data. We’ve grown from $0 to ~$1B run rate and pay ~$60M to over 30K individuals every month.

Why join Handshake now:

  • Shape how every career evolves in the AI economy, at global scale, with impact your friends, family and peers can see and feel

  • Partner hand-in-hand with world-class AI labs, Fortune 500 partners and the world’s top educational institutions

  • Work together with engineers, scientists, operators, and more from Palantir, Meta, Scale AI, and former YC founders

  • Build a massive, fast-growing business with billions in revenue

About The Role

As an Public Sector Account Director, you will be crucial in building and closing deals within the State & Local Government (SLG) sector. You will develop and nurture relationships with key stakeholders, identify opportunities, and drive the sales process from lead generation to deal closure across your named accounts. This role requires in-depth knowledge of the hiring needs and challenges of large and medium-sized SLG employers and an acute understanding of how they function and the human capital challenges they face. It will also require strategic thinking, relationship building, and a strong focus on achieving revenue targets. You will:

  • Develop and cultivate deep relationships with senior executives within prospective human capital departments, among other key stakeholders

  • Meet or exceed annual quota by generating sufficient volume of high-quality meetings with SLG and its large departments and agencies

  • Understand a department or agencies’ business drivers, challenges and pain points

  • Navigate SLG procurement processes and contracting

  • Schedule, manage and run large department meetings with senior economic buyers within high-value SLG Departments

  • Generate well-qualified pipeline and revenue to achieve 100% of annual quota attainment

  • Lead participation in industry events to drive new business development

  • Coordinate large-scale efforts across various departments to drive enterprise-wide agreements

  • Utilize Salesforce.com on a daily basis to manage activity, leads, follow-up and pipeline

You Have

  • Proven knowledge of SLG government procurement process and contracting

  • 5+ years of Account Executive experience selling Saas based solutions into the SLG space

  • Success in pitching and closing six-figure deals

  • Experience navigating and building relationships within large departments and agencies within the SLG

  • Proven ability to negotiate large government contracts while developing off-cycle pipeline and new lead generation

  • Excellent customer-facing skills and ability to manage a room of senior government officials

  • Ability to navigate complex contract structures

  • A strong history of quota attainment and excellent performance

  • Experience preparing account plans and business value narratives

  • Proven ability to collaborate successfully with a go-to-market team

We Offer

Handshake delivers benefits that help you feel supported and thrive at work and in life.

The below benefits are for full-time US employees.

🎯 Ownership: Equity in a fast-growing company

πŸ’° Financial Wellness: 401(k) match, competitive compensation, financial coaching

🍼 Family Support: Paid parental leave, fertility benefits, parental coaching

πŸ’ Wellbeing: Medical, dental, and vision, mental health support, $500 wellness stipend

πŸ“š Growth: $2,000 learning stipend, ongoing development

πŸ’» Remote & Office: Internet, commuting, and free lunch/gym in our SF office

🏝 Time Off: Flexible PTO, 15 holidays + 2 flex days

🀝 Connection: Team outings & referral bonuses

Explore our mission, values, and comprehensive US benefits at joinhandshake.com/careers.

Frequently Asked Questions

What is the salary for the Public Sector Account Director role at handshake?
The listed salary for this Public Sector Account Director position at handshake is USD 260K–300K/yr. This is a remote FullTime role.
Is the Public Sector Account Director job at handshake remote?
Yes, this Public Sector Account Director position at handshake is remote, with team members based in Remote (USA). You can work from home or anywhere in the supported regions.
Is the Public Sector Account Director role at handshake full-time or part-time?
This is listed as a FullTime position. It is posted as a Public Sector Account Director role in the Employer Revenue department at handshake.
Which team or department does the Public Sector Account Director at handshake belong to?
This Public Sector Account Director position is part of the Employer Revenue department at handshake. See the full job description for more information about the team structure and responsibilities.
How do I apply for the Public Sector Account Director position at handshake?
Click the "Apply Now" button on this page. You will be redirected to handshake's official application portal hosted on ashby where you can submit your application directly.
When was the Public Sector Account Director job at handshake posted?
This Public Sector Account Director position at handshake was posted on May 29, 2026. Apply as soon as possible β€” early applications are often reviewed first.
Public Sector Account Director
handshake Β· πŸ’° USD 260K–300K/yr
Apply for this role β†—

You'll be redirected to handshake's official application page on Ashby ATS.