The third Bagley (DD-386) was launched 3 September 1936 by Norfolk Navy Yard; sponsored by Miss Bella Worth Bagley, sister of Ensign Bagley; commissioned 12 June 1937, Lieutenant Commander E. W. Morris in command; and reported to the Atlantic Squadron.

Bagley operated along the east coast and in Cuban waters during the first year following her commissioning. Assigned to Destroyer Division 7, Battle Force, in June 1938, she participated in fleet maneuvers in the Canal Zone, Haitian-Cuban-Florida area, and later on the west coast.

On 7 December 1941 Bagley was moored at Pearl Harbor and when the Japanese planes attacked, she opened fire immediately and assisted in the destruction of several enemy airplanes. Between December 1941 and 30 May 1942, when she arrived in Brisbane, Australia, Bagley performed patrol and escort duties in the Central and Eastern Pacific, taking part in raids on Bougainville (20 February 1942) and Salamaua-Lae (10 March). Between 7 and 30 August 1942 she was at Guadalcanal and took part in the First Battle of Savo Island (9 August) splashing one plane. Following the battle she rescued approximately 450 survivors of Astoria (CA-34), Vincennes (CA-44), and Quincy (CA-39).

From September 1942 until December 1943 Bagley escorted convoys in the South Pacific, except for a brief period supporting the invasion of Woodlark Island (1-2 July 1943). Between 15 December 1943 and 10 February 1944 she performed screening, picket, and escort duties during the invasion of New Britain. Returning to Mare Island Navy Yard 27 February she underwent a complete overhaul and returned to the Pacific 5 May 1944.

Between 13 June 1944 and 24 May 1945 Bagley took part in the bombardment of Tinian and Saipan Islands (13 June-20 July 1944); Battle of the Philippine Sea (19-20 June); bombardment of the Bonin and Volcano Islands (1-2 September); bombardment of Yap Island (7-8 September); invasion of the Southern Palau islands (9 September-6 October); raids on Nansei Shoto, Formosa, and the Northern and Central Philippines (10-21 October); Leyte invasion (22-31 October); Battle of Leyte Gulf (25 October); invasion of Lingayen Gulf (1-23 January 1945); invasion of Iwo Jima (16 February-12 March); and the invasion of Okinawa (25 March-24 May).

On 31 August 1945 Bagley, with Rear Admiral F. E. M. Whiting embarked, arrived at Marcus Island and received the surrender of the island. Between 2 September and 1 November 2945 she served in the Sasebo-Nagasaki area on occupation duty, a fitting end to her distinguished war service.