The third Farragut (DD-348) was launched 16 March 1934 by Bethlehem Shipbuilding Corp., Quincy, MA, sponsored by Mrs. James Roosevelt, daughter in-law of the President; and commissioned 18 June 1934, Commander E. Buckmaster in command.

Since it had been almost fourteen years since a new destroyer was commissioned in the United States Navy, because of the various international treaties limiting naval armament, Farragut devoted much of her early service to development operations, cruising out of her home port Norfolk to the Caribbean and along the east coast. On 26 March 1935, she embarked President F. D. Roosevelt at Jacksonville, FL, and carried him next day to a rendezvous with a private yacht. She escorted the President's yacht on a cruise in the Bahamas; on 7 April, he embarked on her for passage to Jacksonville, where he left the ship 8 April.

Farragut sailed at once for San Diego arriving 19 April 1935 to join Destroyer Squadron 2nd as flagship. Fleet maneuvers on the west coast, training operations in the Hawaiians, and cruises in the summer months to train men of the Naval Reserve in Alaskan waters continued until 3 January 1939, when Farragut sailed for fleet maneuvers in the Caribbean, returning to San Diego 12 April. From 2 October, she was based at Pearl Harbor, intensifying her training operations as war engulfed most of the world. She made two voyages to the west coast to screen carriers to Pearl Harbor, and from 1 August 1941, was almost constantly at sea for exercises with carrier task forces.

Farragut was berthed in a nest of destroyers in East Loch, Pearl Harbor, at the time of the Japanese attack 7 December 1941. Her engineering officer, senior on board at the time, got her underway, and as she sailed down the channel, she kept up a steady fire, driving away all attackers save one plane which strafed her topsides, causing only slight damage, and injuring none of the crew. Through March 1942, Farragut operated in Hawaiian waters, and from Oahu to San Francisco, on antisubmarine patrols and escort duty.

On 16 April 1942, Farragut sortied from Pearl Harbor with the Lexington (CV-2) task force, bound for the Coral Sea and a rendezvous with the Yorktown (CV-5) task force. Together these forces challenged Japanese attempts to take Port Moresby, New Guinea in the Battle of the Coral Sea from 4 to 8 May 1942 halting the hitherto uninterrupted Japanese push to the southeast, and saving Australia and New Zealand from threatened invasion. For the first 2 days of the battle Farragut sailed with the Attack Force, while the carriers in another group launched air strikes on Tulagi. On 6 June, all ships were united as TF 17, and sailed to the northwestward to make contact with the Japanese Port Moresby Invasion Group. Next day, as it became apparent that a carrier battle was about to develop, Farragut was detached in the Support Group assigned to continue the search for the Japanese invasion forces as the main body of the fleet prepared for a key strategic victory in the air action. Farragut's group came under heavy air attack that afternoon, but drove the Japanese off, splashing at least five of the enemy, and receiving no damage to any ship.

Farragut arrived at Cid Harbor, Australia, 11 May 1942, and until returning to Pearl Harbor 29 June, called at Brisbane, Noumea Suva, Tongatabu, and Auckland while on escort duty. She next sortied from Pearl Harbor 7 July 1942, in the Saratoga (CV-3) task force, bound for action in the Solomons. She served as screening ship and plane guard during the air operations covering the assault on Guadalcanal 7 August, then patrolled the eastern Solomons to protect sea lanes to Guadalcanal. On 24 and 25 August the carrier she guarded engaged Japanese forces in the air Battle of the Eastern Solomons, turning back a major effort of the Japanese to reinforce Guadalcanal and Tulagi, and attack American sea and land forces so as to recapture the islands.

The destroyer remained in the southwest Pacific, patrolling off Guadalcanal to guard unloading transports, and escorting convoys from Australia to Espiritu Santo, Noumea, and the Fiji Islands. She returned to Pearl Harbor 27 January 1943, and after a west coast overhaul and training, arrived at Adak 16 April. She patrolled Alaskan waters until 11 May when she screened transports landing troops on Adak from submarine attack. Next day she made several depth charge attacks on an enemy submarine and she continued antisubmarine patrol off the Aleutians through June. Farragut patrolled and blockaded off Kiska from 5 July, joining in the bombardment of the island many times in the days before the landings of 15 August. She continued to protect the troops ashore at Kiska until 4 September, when she left Adak in convoy for San Francisco and a brief overhaul.

Farragut put to sea from San Diego 19 October 1943, bound for training in the Hawaiian Islands and at Espiritu Santo. Again guarding carriers, she took part in the air operations covering the landings on Tarawa 20 November, and screened the carriers until the task force shaped course for Pearl Harbor 8 December. The destroyer continued on to the west coast for a brief repair period and training, sailing from San Diego 13 January 1944 for action in the Marshalls. During the assaults on Kwajalein and Eniwetok, she screened carriers, patrolled, and conducted antisubmarine searches, then sailed for air strikes on Woleai and Wakde. Late in April, she was off New Guinea as the carriers supported the landings in the Hollandia area, and through May joined in training operations out of Majuro.

From her arrival off Saipan 11 June 1944, Farragut guarded the carriers covering the landings of 15 June, bombarded the shores of Saipan and Guam, and served as radar picket through the Battle of the Philippine Sea on 19 and 20 June. With this threat to the Marianas operation balked and the Japanese Navy decisively defeated, Farragut sailed to replenish at Eniwetok 28 June to 14 July. On 17 and 18 July, she closed the beach at Agat, Guam, to provide covering fire for underwater demolition teams preparing for the assault on the island. After screening a cruiser to Saipan she returned to Guam 21 July to patrol seaward of the Fire Support Group covering the assault landings. On 25 July, she joined in the bombardment of Rota, and 5 days later cleared for overhaul at Puget Sound Navy Yard.

Farragut arrived at Ulithi 21 November 1944, and sailed 4 days later to screen a group of oilers serving the fast carrier task force as it sent strikes against Taiwan and Luzon in preparation for the assault on Lingayen. Based on Ulithi, she served with this group as it supported the carriers in their operations of the Iwo Jima and Okinawa invasions, then from 25 to 28 April 1945 served on carrier screening duty for air operations on islands of the Ryukyus not yet invaded. From 11 May to 6 August, she escorted convoys between Ulithi and Okinawa, and during the last 2 weeks of May, served on radar picket duty at Okinawa.

The destroyer was homeward bound from Saipan 2I August 1945, arriving at the Brooklyn Navy Yard 25 September. There she was decommissioned 23 October 1945, and was sold 14 August 1947.

Farragut received 14 battle stars for World War II service.