1966–1969

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.

In late January 1968 Flasher deployed with the fleet assembled after the USS Pueblo was captured by the North Koreans. Her station was in the Sea of Japan off the harbor of Wonsan, NK. While patrolling she encountered a small ice flow that snapped off the top of a periscope. Flasher proceeded to Guam for 9 days to have the periscope replaced and then proceeded back to her station off North Korea. After leaving station Flasher obtained permission to have a port call at Yokosuka, Japan before sailing for her home port of Pearl harbor Hawaii. For this deployment Flasher was awarded the Armed Forces Expeditionary Medal and the Korean Defense Service Medal.

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. Flasher was awarded her second consecutive Battle Efficiency "E" on 1 July 1969. On 2 December 1969 Flasher was awarded her first Meritorious Unit Commendation for her service during the period March 1967 through August 1968.

1970–1979

On 15 June 1970 Flasher commenced her first major overhaul at Pearl Harbor Naval Shipyard, which was completed by 12 June 1971. 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. On 1 July 1972 Flasher was awarded her third Battle Efficiency "E" for overall combat excellence, and on 13 July 1972 received a visit from Secretary of the Navy John Chafee. On 19 August 1972 Flasher was awarded a Presidential Unit Citation, at a ceremony, where CDR R.F. Bacon assumed command. Bacon would later go on to become Vice Admiral and Assistant Chief of Naval Operations for Undersea Warfare. Flasher then participated in the RIMPAC 72 exercise that September.

On 2 March 1973 Flasher was awarded a Navy Unit Commendation for her operations in 1970–1971. She commenced another WESTPAC deployment in early 1973, visiting Yokosuka, Japan, Guam, and Hong Kong before returning to Pearl Harbor on 24 December 1973. During this tour, on 1 July 1973, she was awarded her fourth Battle Efficiency "E" for overall combat excellence. In June 1974 Flasher completed a two-month special operation.

Flasher commenced her second overhaul (Refueling and Overhaul) at Mare Island Naval Shipyard on 11 January 1975, changed homeport to Mare Island, and shifted administrative command to Submarine Squadron 3. The overhaul completed on 16 December 1976, she changed homeport to San Diego, California, on 22 December 1976.

In August 1977 she attended the Seattle Seafarer Festival.

"Flasher" completed a 3-month Mid-Pac / special operation April to June 1978.

In January 1979 Flasher commenced a Selected Restricted Availability (SRA) at Mare Island Naval Shipyard, which was completed on 29 March 1979. In June 1979 she attended the Portland Rose Festival. On 1 July 1979 she was awarded her fifth Battle Efficiency "E".

1980–1992

On 12 November 1980 she was awarded her second Meritorious Unit Commendation for the period November 1979 through May 1980, and on 5 November 1982 was awarded a third Meritorious Unit Commendation for the period July 1981 through January 1982. The crew earned the Navy Expeditionary Medal for actions taken during this period.

"Flasher" completed a 3-month Mid-Pac / special operation August to November 1982.

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. The crew earned the Navy Expeditionary Medal for actions taken during this period.

Flasher completed her last WESTPAC deployment, with visits to Guam; Yokosuka, Japan; Korea; and Hong Kong, in April 1990.

Flasher completed a two-month special operation in August–October 1990, and another in March–May 1991.

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.