She was launched on 9 April 1944, sponsored by Miss Florence King, daughter of the Chief of Naval Operations, Admiral Ernest J.

Following training at Naval Submarine Base New London in Groton and at Newport, Rhode Island, Blenny got underway for Key West, Florida, on 29 August 1944.

On 6 December, she escaped unscathed from another close call when a low-flying Japanese plane dropped two bombs that near-missed Blenny.

In the morning, she made a surface gun attack on a Japanese 300-gross register ton "sea truck" — the U.S. term for a type of small cargo ship — and sank it.

On 23 December, Blenny torpedoed and sank what she thought was a 10,000-ton transport which after the war was identified as the Japanese 4,156-gross register ton cargo ship Kenzui Maru.

On the night of 26 February 1945, she encountered the Japanese 10,238-gross register ton tanker Amato Maru and sank her with a spread of torpedoes.

On 28 February 1945, Blenny received orders to put into Subic Bay on Luzon to reload torpedoes, and she arrived there on 2 March.

She sighted no Japanese ships during her time in the South China Sea and returned to Subic Bay on 16 May 1945 to take on additional fuel.

She had to make her approach to an attack position in relatively shallow water, so she flooded down and backed awash toward the shore and the submarine chaser while a sailor on her fantail took depth soundings with a lead line.

Departing Fremantle, she shaped a course for a patrol area in the Java Sea and north from there to the eastern coast of Japanese-occupied British Malaya.

For the remainder of the patrol, Blenny encountered only sampans, junks, and the like, sinking a large number of them after ascertaining their nationality and seeing to the safety of their crews.

On 30 July 1947, she got underway from San Diego on a United States Naval Reserve training cruise to the Pacific Northwest, during which she visited ports in Washington and British Columbia in Canada.

In July 1950, she began a voyage to Pearl Harbor, then, after participating in fleet maneuvers off Hawaii, returned to San Diego early in August 1950.

After its completion, she operated along the U.S. West Coast until 30 April 1952, when she got underway for Pearl Harbor, then continued across the Pacific for a cruise in the Far East, arriving in Yokosuka, Japan, on 24 May 1952.

After stops at Chichi Jima in the Volcano Islands and Pearl Harbor, she arrived at San Diego early in November 1952.

Blenny resumed operations along the U.S. West Coast until she was reassigned to the United States Atlantic Fleet in the spring of 1954.

She transited the canal on 24 May 1954 and headed for Naval Submarine Base New London at Groton, Connecticut, which she reached on 9 June 1954.

Operating from Naval Submarine Base New London, Blenny participated from 1954 until the early 1960s in U.S. Atlantic Fleet, North Atlantic Treaty Organization (NATO), and antisubmarine warfare exercises, in addition to operating with a U.S. Navy submarine development group engaged in evaluating new equipment.

In the early 1960s, Blenny began making periodic deployments to the Mediterranean Sea for duty with the United States Sixth Fleet, alternating between tours of duty with the Sixth Fleet and extended assignments in the western Atlantic Ocean, where she conducted test and evaluation operations and took part in antisubmarine warfare training.