After shakedown and preliminary training off the United States East Coast, Runner departed New London, Connecticut, on 5 April 1945, conducted intensive training at Key West, Florida, and Balboa, Panama Canal Zone, and arrived at Pearl Harbor, Hawaii, on 21 May 1945.

Runner′s second war patrol began a week prior to the Japanese capitulation on 15 August 1945, and by the time she arrived on station off the east coast of Honshū, peace had come.

A few weeks later, in company with other vessels of Submarine Squadron 6, Runner proceeded south, arriving for duty at Balboa, Panama Canal Zone, on 14 February 1946.

For the next three years, she was based at the Panama Canal Zone and participated in annual fleet exercises in the Caribbean Sea.

Runner began 1968 by providing services for the Underwater Demolition Team school at Little Creek, Virginia, and antisubmarine warfare training off the U.S. East Coast.

She returned to Norfolk on 31 July 1968 having visited ports in Spain and Portugal, and participating in the NATO exercise Dawn Patrol.