Runner's keel was laid down on 8 December 1941 by the Portsmouth Navy Yard at Kittery, Maine.

Following shakedown from New London, Connecticut, Runner departed the United States East Coast in late 1942, transited the Panama Canal, and arrived at Pearl Harbor, Hawaii on 10 January 1943.

It later was determined that in fact Runner had torpedoed and damaged the Imperial Japanese Army hospital ship Buenos Aires Maru on 24 April 1943.

Captured Japanese records examined after World War II indicated that she sank the cargo ship Seinan Maru on 11 June 1943 in Tsugaru Strait off Hokkaidō and on 22 June 1943 was attacked and apparently damaged by Imperial Japanese Navy forces.

This article incorporates text from the public domain Dictionary of American Naval Fighting Ships.