Ponchatoula was laid down at the New York Shipbuilding Corporation, Camden, New Jersey, on 1 March 1954, launched on 9 July 1955, sponsored by Mrs.

Rotated regularly to the western Pacific, Ponchatoula was homeported at Pearl Harbor in early 1958 and received her introduction to support under hostile conditions while operating with 7th Fleet units during the Quemoy-Matsu Crisis in the fall of that year.

Repeating that support with Faith 7 in 1963, she shifted to combat operations in October 1964 and deployed to the South China Sea to refuel ships employ the coast of Vietnam.

The Chancellorsville suffered a steering casualty during underway replenishment operations and heeled sharply to port, ramming the Ponchatoula's starboard side at the Bridge, then sliding down the starboard side of the ship, buckling the upper deck plates of the Ponchatoula to the engine house and damaging the Chancellorsville's hurricane bow and sonar dome.

Ponchatoula was struck from the Naval Vessel Register on 31 August 1992; her title was transferred to MARAD on 1 May 1999 for lay-up in the National Defense Reserve Fleet, Suisun Bay, Benicia, California.