It is a division of the Washington State Department of Transportation (WSDOT) and operates 10 routes serving 20 terminals within Puget Sound and in the San Juan Islands.

[7] The new system was operated by the Washington State Toll Bridge Authority, which ordered ten new vessels that could carry 60 to 100 vehicles.

A set of revenue bonds were also issued to purchase the 16 vessels and 20 terminals of the Puget Sound Navigational Company for a total of $4.94 million.

[8] A route between Port Townsend and Keystone on Whidbey Island was launched in June 1974 to replace a privately-run service that had lost its franchise.

The loss of workers who retired, transferred, or were fired during the pandemic caused delays and trip cancellations as service and ridership began to recover in 2021 and 2022, while vessel replacement also ran behind schedule.

[12] As mitigation for the delay in restoring the Seattle–Bremerton run's second vessel, WSF funded additional trips on the parallel Kitsap Fast Ferries that serves both terminals.

[21] Onboard food service, primarily through the ship galley and vending machines, is operated by contractor Sodexo Live.

[29][30] The program was originally expected to begin in 2022 with a new boat constructed by Vigor Industrial, but cost overruns and disagreements led to delays.

[31] Bids for the hybrid-electric ferries, which will carry 164 vehicles and 1,500 passengers, were opened to non-Washingtonian shipbuilders in 2024 with invitations sent to 15 interested companies.