With DesRon 1, Farragut was transferred in 1935 to the Pacific, where the squadron took part in the U.S. Fleet's peacetime maneuvers and training. Operating from Pearl Harbor beginning in 1939, Farragut was moored there with the squadron on the morning of 7 December 1941 when Japanese planes attacked.
Early wartime missions included patrol and escort duties off Hawaii and California. In early May 1942, the destroyer as assigned to Rear Admiral Kinkaid’s Attack Group—cruisers Minneapolis, New Orleans, Chester, Portland and Astoria with destroyers Phelps, Dewey, Monaghan and Aylwin—during the Battle of the Coral Sea.
In August, with Phelps, Macdonough and Worden, she screened aircraft carriers during Operation “Watchtower,” the invasion of Guadalcanal and Tulagi, and with these ships during the Battle of the Eastern Solomons, was joined in Saratoga‘s screen by Dewey, Dale, Bagley and Patterson.
During the rest of the Guadalcanal Campaign she was mainly employed on patrol and escort missions. Following overhaul in early 1943, she was sent to Alaskan waters, where she took part in the Attu and Kiska operations in May and August. In November 1943 and January-February 1944, Farragut was part of the armada that seized bases in the Gilbert and Marshall islands. She then moved south to support landings along the north shore of New Guinea before returning to the central Pacific to participate in the invasions of Saipan and Guam and in the Battle of the Philippine Sea, during June and July 1944.
Later in the year, Farragut was assigned to screen a force of oilers that sustained the fleet during its assaults on Japanese positions in the western Pacific. Though escort missions occupied most of her remaining World War II service, she was also employed on radar picket duty during the Okinawa campaign in April and May 1945.
Soon after the fighting ended, Farragut was sent back to the United States. She arrived at the New York Navy Yard in late September 1945, was decommissioned a month later and sold for scrapping in August 1947.
Farragut earned 14 battle stars for her service in World War II.