Established in early-1943 as a P-47 Thunderbolt fighter squadron, the 374th Fighter Squadron trained under I Fighter Command in the mid-Atlantic states. Also flew air-defense missions as part of the Philadelphia Fighter Wing. Deployed to the European Theater of Operations (ETO) as part of the 361st Fighter Group, being assigned to VIII Fighter Command in England, November 1943.

The unit served primarily as an escort organization, covering the penetration, attack, and withdrawal of B-17/B-24 bomber formations that the USAAF sent against targets on the Continent. The squadron also engaged in counter-air patrols, fighter sweeps, and strafing and dive-bombing missions. Attacked such targets as airdromes, marshalling yards, missile sites, industrial areas, ordnance depots, oil refineries, trains, and highways. During its operations, the unit participated in the assault against theLuftwaffe and aircraft industry during the Big Week, February 20–25, 1944, and the attack on transportation facilities prior to the Normandy invasion and support of the invasion forces thereafter, including the Saint-Lô breakthrough in July.

The squadron supported the airborne attack on the Netherlands in September 1944 and deployed to Chievres Airdrome, (ALG A-84), Belgium between February and April 1945 flying tactical ground support missions during the airborne assault across the Rhine. The unit returned to Little Walden and flew its last combat mission on April 20, 1945. Demobilized during the summer of 1945 in England, inactivated in the United States as a paper unit in October.