The contract to build her was awarded to the Electric Boat Division of General Dynamics Corporation in Groton, Connecticut on 9 June 1960 and her keel was laid down on 14 April 1961.

Vice Admiral Elton W. Grenfell, then Commander Submarine Force, U.S. Atlantic Fleet (ComSubLant), delivered the principal address.

After commissioning, Flasher arrived at new her home port of Pearl Harbor, Hawaii, on 23 September 1966, under command of CDR Kenneth M. Carr.

On 7 October 1966 she received a visit from the Director General of the Japanese Defense Agency Mr. Elkichi Kambayashiyama, in company with COMSUBPAC Rear Admiral John H. Maurer.

Flasher sailed for her first Western Pacific (WESTPAC) deployment on 25 April 1969, and was awarded her first Battle Efficiency "E" for overall combat excellence on 4 July 1968.

In November 1971 Flasher commenced another WESTPAC deployment, visiting Guam, Mariana Islands; White Beach, Okinawa; Yokosuka, Japan; Subic Bay, Philippines, and Hong Kong, before returning to her home port in June 1972.

She commenced another WESTPAC deployment in early 1973, visiting Yokosuka, Japan, Guam, and Hong Kong before returning to Pearl Harbor on 24 December 1973.

In January 1979 Flasher commenced a Selected Restricted Availability (SRA) at Mare Island Naval Shipyard, which was completed on 29 March 1979.

Flasher commenced her third overhaul at Mare Island Naval Shipyard on 9 May 1983, which was completed on 26 March 1985, and she shifted homeport back to San Diego, California.

In March 1986 Flasher began another WESTPAC deployment, and visited Yokosuka, Japan; Guam; and Subic Bay, completing the voyage in August 1986.

Flasher was awarded her Fourth Meritorious Unit Commendation in 1991 for the ship's last two-month special operation, and on 18 June 1991 an Inactivation Ceremony was held at the Naval Base Point Loma, San Diego, California.

USS FLASHER successfully accomplished an extremely difficult, demanding, and most sensitive operation of exceptional value and lasting significance to the readiness posture of the United States.