International Radio Call Sign: November-Juliet-Bravo-Hotel
Growler was laid down on 15 February 1955 by the Portsmouth Naval Shipyard of Kittery, Maine. She was launched on 5 April 1958 sponsored by Mrs. Robert K. Byerts, widow of Commander Thomas B. Oakley, Jr., who commanded the third Growler on her 9th, 10th, and fatal 11th war patrols. Growler commissioned at Portsmouth on 30 August 1958 with Lieutenant Commander Charles Priest, Jr., in command.
After training exercises off the East Coast Growler sailed south for her shakedown cruise, arriving at the Roosevelt Roads Naval Station, Puerto Rico, on 19 February 1959. After a brief run back to Portsmouth, she returned to the Caribbean Sea in March to train in launching Regulus I and Regulus II nuclear cruise missiles, assisted by USS Runner (SS-476), which was one of several submarines with Regulus guidance equipment. Growler returned to Portsmouth 19 April via Fort Lauderdale, Florida, and New London, Connecticut.
Growler then proceeded to the Pacific via Norfolk, Virginia, Key West, Florida, and the Panama Canal, putting in at Pearl Harbor on 7 September to serve as flagship of Submarine Division 12. At Pearl Harbor the guided missile sub participated in a variety of battle and torpedo exercises as well as missile practice before beginning her first Regulus Deterrent Mission. On this mission, which lasted from 12 March to 17 May 1960, Growler departed Hawaii with a full store of Regulus sea-to-surface missiles, armed with nuclear warheads, and patrolled under a strict cloak of secrecy. Their patrols could last two months or more at a stretch and required them to remain submerged for hours and even days—which at first hardly seems difficult when compared to the patrols of nuclear-powered ballistic missile submarines, but was a strain for the crew of a much smaller diesel boat. It is traditional that the log entries for 00:00 (midnight) on New Year's Day be made in verse. On 1 January 1961, during Growler's second patrol, Lieutenant (j.g.) Bruce Felt wrote: "Not our idea of fun and good cheers/But doing our job to ensure many New Years."
From May 1960 through December 1963 Growler had made nine such deterrent mission patrols, one of which, the fourth, terminated at Yokosuka, Japan, on 24 April 1962, as the Navy displayed one of its newest weapons.
Returning to Mare Island, California, Growler decommissioned 25 May 1964 and was placed in reserve. She was initially moved to the Inactive Fleet section in the Puget Sound Naval Shipyard in Bremerton, Washington and was later relocated to the Philadelphia Naval Shipyard. She was struck from the Naval Vessel Register on 1 August 1980 and was scheduled to be used as a torpedo target. However, on 8 August 1988, Congress awarded the hulk to Zachary Fisher, Chairman of the Intrepid Sea, Air & Space Museum in New York City.
Due to the renovations to the entire Intrepid Sea, Air & Space Museum complex, including the USS Intrepid and Pier 86 the Growler was towed to Brooklyn for repairs. Holes found rusted in the hull complicated matters and pushed repair costs past $1.5 million. The Growler returned to Pier 86 in late February 2009, and was re-opened to the public on 21 May 2009, during the Intrepid museum "Fleet Week 2009" celebration.