Tills was laid down on June 23, 1943, by the Western Pipe and Steel Company at San Pedro, Los Angeles, launched that October, and commissioned on August 8, 1944. She belonged to Escort Division 53 and spent her first months working trials and shakedown runs off San Diego. By October she was sailing for Pearl Harbor in the screen of an escort carrier task group, and from January 1945 onward she pulled hunter-killer duty in the Marshalls. The pattern was relentless. Sail east by day, west by night, four hundred miles out from Eniwetok, scanning for Japanese submarines on the supply lanes between Hawaii and the central Pacific. On April 20 a typhoon scattered the task group with seventy-knot winds and seas heavy enough to ground the carrier aircraft. Three days later the storm let go. The destroyer escorts limped back to base.

On May 3, 1945, Tills made port at Ulithi, then joined a convoy bound for the Ryukyus. En route she came across an abandoned Japanese patrol boat and finished it off with gunfire and depth charges. She dropped anchor off Hagushi Beach on May 10 in the thick of the Okinawa campaign. Two days later, when enemy aircraft were reported in the area, her 40-millimeter Bofors guns opened up on two planes emerging from a smoke screen until a sharp-eyed lookout shouted that the planes were friendly. The guns fell silent; the aircraft flew off, undamaged. The crew counted it a near miss they would never forget. Tills then screened Carrier Division 22 as the escort carriers struck Sakishima, a Japanese refueling base feeding the kamikaze offensive between Kyushu and Formosa. She was off Guam in dry dock when the bombs fell on Hiroshima and Nagasaki, still in dock when Japan surrendered on August 15.

Tills was decommissioned in June 1946 and tied up in the St. Johns River, but the Navy could not afford to lose her for long. Reactivated in 1947, she was sent to Miami to train naval reservists, working her way up the East Coast from Boston to Panama. In November 1950 she was placed back in full commission at Charleston, South Carolina, with Lieutenant Commander Elmo R. Zumwalt in command, a young officer who would one day serve as Chief of Naval Operations. Through the 1950s Tills trained reservists, cruised to Lisbon and Cadiz, took part in exercises with names like Convex III and Emigrant. In October 1961, amid rising Cold War tensions following the Bay of Pigs, she was recommissioned at Norfolk and held station through the Cuban crisis. When the danger eased in August 1962 she went back to Portland, Maine, and was decommissioned again.

For the rest of her career Tills did the unglamorous work that keeps a Navy ready: weekend reserve cruises out of Portland, antisubmarine exercises up and down the St. Lawrence Seaway, joint maneuvers with the Canadians. In 1964 she made a four-day port call at the New York World's Fair and served as a patrol ship for the annual Starboat Yacht Races off Winthrop, Massachusetts. She visited the Rockland Seafood Festival in August. These were the small dignities of a ship near the end of her service: a parade, a fair, sailors leaning on the rail in port. On September 23, 1968, Tills was found unfit for further service and struck from the Naval Vessel Register. On April 3, 1969, she was towed out into the Atlantic off Virginia and sunk by Navy weapons as target practice, ending the long second life of a ship named for a man who never saw twenty-five.