The contract to build Billfish was awarded to the Electric Boat Division of General Dynamics Corporation in Groton, Connecticut, on 15 July 1966 and her keel was laid down on 20 September 1968.

Upon her commission, she was assigned to Submarine Development Group Two, based in Groton, Connecticut.

She was deployed to the Mediterranean, participating in fleet exercises and tactical and sonar development tests.

Billfish was one of the few submarines fitted to carry the Mystic class deep submergence rescue vehicle during the 1980s.

Her scrapping was via the Nuclear-Powered Ship and Submarine Recycling Program at Puget Sound Naval Shipyard in Bremerton, Washington, was completed on 26 April 2000.