S-29′s keel was laid down on 17 April 1919 by the Bethlehem Shipbuilding Corporation's Fore River Shipyard in Quincy, Massachusetts.

After duties in the northeastern United States operating from New London, Connecticut, in 1924, S-29 visited Hawaii from 27 April to 30 May 1925.

Operating therrafter mainly from Mare Island, San Diego, and San Pedro, California until 1931, S-29 also served in the Panama Canal area from February to March 1926, visited Hawaii in the summers of 1927 and 1928, served in the Panama Canal area during February 1929, and again visited Hawaii during the summer of 1930.

S-29 then operated at Pearl Harbor until 16 June 1939, when she departed bound for New London, which she reached on 23 August 1939.

The U.S. Navy struck S-29 from the Naval Vessel Register in 1946 and sold her in the United Kingdom to H. G. Pound on 24 January 1947 for scrapping.