Following underway trials, training, and shakedown in the Portsmouth, New Hampshire, and New London, Connecticut, areas, Sea Poacher transited the Panama Canal and arrived at Pearl Harbor on 25 October 1944.

Although her first two war patrols were unproductive, during the third, conducted in the Kuril Islands area, Sea Poacher torpedoed and sank a Japanese trawler and, four days later, sent two fishing boats to the bottom in a surface attack.

On 10 July 1952, while operating in the Key West area, the submarine had the unique experience of rescuing a blimp which had suffered an engine casualty and was floating helplessly in the water.

The submarine promptly came to the aid of the stricken airship and proceeded to tow it the 40 miles (64 km) back to its base at Naval Air Station, Boca Chica, Florida.

In 1969, Sea Poacher concluded her service with a 3+1⁄2-month deployment to the eastern and northern Atlantic areas to participate in antisubmarine training exercises with units of the Spanish and Portuguese navies.