Ronquil was laid down on 9 September 1943 at the Portsmouth Navy Yard, in Kittery, Maine; launched on 27 January 1944, sponsored by Mrs. C. M. Elder; and commissioned on 22 April 1944.

Her fourth war patrol from 11 March to 23 April 1945, brought her no worthwhile enemy targets but resulted in the rescue of 10 Army aviators from a B-29 bomber downed between the Bonins and Japan.

On her return to San Diego, she resumed local operations before beginning a three-year period of intensive training in offensive and antisubmarine warfare, embodying lessons learned during World War II as well as new postwar developments.

Ronquil entered Mare Island Naval Shipyard in May 1952 for decommissioning and "Guppy IIA" modernization: Her hull and sail were streamlined for greater submerged speed.

She arrived at Yokosuka before sailing on to Tokyo on 19 July to take part in the "Black Ship Festival" commemorating Commodore Matthew Perry's opening of Japan in 1852.

The next 2 years were devoted to operations off the west coast of the United States; on 31 July 1957, the submarine again deployed to the Far East for 7 months.

During July and August 1960, she participated in extensive antisubmarine exercises in the eastern Pacific with United States and Canadian forces.

The submarine departed San Diego in November 1963 for duty with the United States Seventh Fleet; on her return to California, she again resumed operations off the west coast.

This was interrupted in August 1967, when Ronquil played the part of the fictional USS Tigerfish (SSN-509) in the motion picture Ice Station Zebra.

At the end of January 1970 Ronquil began a period of repair and overhaul, followed by training and fleet exercises in the eastern Pacific.