The third Ericsson (DD-440) was launched 23 November 1940 by Federal Shipbuilding and Drydock Co., Kearny, NJ; sponsored by Mrs. Ruth E. Wallgren, great-great-grandniece of John Ericsson; and commissioned 13 March 1941, Lieutenant Commander G. E. Sage in command.

After shakedown, Ericsson arrived at Norfolk, her home port, 2 May 1941, and at once began operations along the east coast and to Bermuda, training Naval Reserve midshipmen, exercising with submarines, making tests of her equipment and machinery, and joining in battle practice. In the fall of 1941, she twice voyaged to Newfoundland and Iceland, escorting convoys, continuing this service after the United States entered the war. Patrolling off Argentia 15 January 1942, she sighted the life rafts of sunken SS Dayrose, from which she rescued two survivors. Her rescue work also include, patrol service during the rescue of survivors from the torpedoed Coast Guard cutter Hamilton on 30 January 1942.

Ericsson escorted a convoy to the Canal Zone in May 1942, and another to Ireland and Scotland in June. Through the remainder of the summer, she escorted convoys along the east coast and in the Caribbean and took part in exercises, and also patrolled out of San Juan, P.R. On 24 October, she sortied from Norfolk for the invasion of North Africa, and took part in the landings on the coast of French Morocco 8 November. For the next week she offered direct fire support to the troops ashore, assisting in knocking out four enemy batteries on a ridge commanding the landing area the first day; she also screened transports lying off the beach. Ericsson returned to Norfolk 26 November.

After a brief overhaul at Charleston, Ericsson returned to patrol and escort duty in the Caribbean and to Recife and Trinidad. In May 1943, she made the first of five convoy escort voyages to Casablanca from east coast ports, between which she joined in training, and patrolled the western Atlantic. On 11 February 1944 she arrived at Gibraltar for duty in the Mediterranean, and through the next 6 months, operated primarily to support the troops fighting the bitter campaign for Italy. She escorted convoys and carried passengers between north African and Italian ports, bombarded points near the fiercely contested Anzio area and in the Gulf of Gaeta, patrolled off anchorages and harbors, and joined in exercises preparing for the invasion of southern France.

On 13 August 1944, Ericsson sortied from Malta in a task group composed primarily of British ships, but including one French ship and the remainder of Ericsson's division. This group covered one section of the amphibious landings on southern France from 15 to 17 August, and Ericsson, after screening HMS Ramillies to Corsica, returned to join an American task group and fire bombardments along the French coast. She also served on patrol, and on 27 August intercepted a trawler, in which the crew of a German submarine, previously grounded and scuttled in the area, were attempting to escape through the American patrol line. Fifty prisoners were thus taken. Ericsson remained in the Mediterranean for patrol and escort assignments until 11 November, when she sailed from Oran to the Azores on escort duty. Upon her return to Gibraltar, she got underway for New York City, arriving 30 November for overhaul.

After refresher training, Ericsson escorted a convoy to Oran from the east coast in April 1944, and while returning to Boston, on 5 May joined Atherton (DE-169) and Moberly (PF-63) in a submarine hunt off Block Island. With other ships joining from time to time, and two airships helping to determine the final sinking, the three ships found and sank U-853. At Boston from 6 May to 18 June, Ericsson prepared for Pacific service, and after training in the Caribbean and at Pearl Harbor, escorted a group of transports to Saipan, arriving 13 September 1945.

Ericsson sailed to Okinawa, Japan, the Philippines, and back to Japan again on escort duty until leaving Sasebo astern 14 October 1945, bound with servicemen eligible for discharge to San Diego. She continued to Charleston, arriving 5 December 1945, and there was decommissioned 15 March 1946 and placed in reserve.

Ericsson received three battle stars for World War II service.