After shakedown off southern California, the new destroyer minelayer sailed from San Francisco on 25 November 1944 via Pearl Harbor for Ulithi, arriving on 3 February 1945. Underway from Ulithi on the morning of 8 February, Lindsey steamed toward Iwo Jima. Operating off Iwo from 17 to 19 February, Lindsey knocked out six enemy guns ashore and provided covering fire as minesweepers cleared the harbor. On the 23rd she returned to Ulithi to prepare for landings on Okinawa.

Underway on 19 March, Lindsey arrived off Okinawa on 24 March and swept the harbor for the inbound transports. Then as the Marines gained a foothold, the ship bombarded Japanese gun installations and transferred wounded soldiers to hospital ships. On the afternoon of 12 April, Lindsey experienced a mass kamikaze attack. Her gunners scored repeated hits on seven onrushing dive bombers, but two “Vals,” damaged and out of control, crashed Lindsey, killing 57 sailors and wounding 57 more. The explosion from the second Val ripped some 60 feet off her bow. Only the “all back full” ordered by Commander Chambers prevented the pressure of inrushing water from collapsing the fireroom bulkhead and sinking the ship.

Towed to Kerama Retto the same night, Lindsey remained in the lagoon for two weeks repairing battle damage. On 28 April, she departed under tow for Guam, where, after arrival on 6 May, she received a temporary bow. She sailed under her own power on 8 July for the East Coast via Pearl Harbor and the Panama Canal, arriving at Norfolk on 19 August 1945.

After extensive repairs at the Norfolk Naval Shipyard, Lindsey steamed on 6 March 1946 for Charleston, South Carolina and arrived the next day. Lindsey decommissioned 25 May 1946 and entered the Atlantic Reserve Fleet. She is berthed at Philadelphia into 1969.

Lindsey received two battle stars for World War II.