[4][5] The squadron was stationed at several bases in Florida before settling at Lake Charles Army Air Field in November 1943.

Just before disbanding, the 336th Group began to receive Douglas A-26 Invaders to replace its Marauders[5][6] The second predecessor of the squadron was activated at Mountain Home Air Force Base, Idaho on 16 April 1951 as the 580th Aerial Resupply Squadron and assigned to the 580th Air Resupply and Communications Group.

"[4] The squadron was equipped with a mix of twelve Boeing B-29 Superfortress, four Fairchild C-119 Flying Boxcar, and four Grumman SA-16 Albatross aircraft.

[8] The squadron's mission included infiltration, resupply, and exfiltration of guerillas behind enemy lines and the aerial delivery of psychological warfare materials.

Although the tests proved the system was feasible, safety considerations with such a large aircraft flying so close to the ground resulted in the program being dropped.

[8] In September 1952, the squadron moved to Wheelus Field, Libya, with the aircrews ferrying their planes, while the ground echelon proceeded by ship.

During this time it was the wing's first squadron to transition to the North American F-100D and F-100F Super Sabre, although it also continued to fly Republic F-84F Thunderstreaks.

On 1 April 1959, it was inactivated along with the remainder of the 366th Wing as Tactical Air Command reduced its fighter units due to budget limitations.

[14][15] On 15 June 1963, the squadron ended all alert and operational commitments and began preparing their Thunderstreaks for ferrying to Holloman Air Force Base, New Mexico.

[4][16] The squadron deployed to Da Nang Air Base, South Vietnam, on 5 February 1966 as the USAF built up its forces there.

[11] With the continued drawdown of United States forces from Vietnam, the 37th was inactivated and its assets were transferred to the 12th Tactical Fighter Wing, which moved without personnel or equipment from Cam Ranh Bay Air Base on 1 April 1970.

[11] The 480th was inactivated on 17 November 1971 and its aircraft redistributed to other units in Southeast Asia as Phu Cat was transferred to the Republic of Vietnam Air Force.

[4][11] In November 1967, a member of the squadron, Captain Lance Sijan, ejected from his disabled aircraft and was badly injured in North Vietnam.

[18] The 480th was reactivated on 15 November 1976 as part of the 52nd Tactical Fighter Wing at Spangdahlem Air Base, Germany, again flying the F-4D Phantom II.

[4] In April 1987, the 480th began receiving the General Dynamics F-16C Fighting Falcon to replace its aging F-4Es in the killer role.

[21] A little over a month later, it began transferring its F-16C and D Block 30 aircraft to the 178th Fighter Group of the Ohio Air National Guard.

[25] Pilots who did not deploy for Operation Inherent Resolve were impacted by the 2013 United States budget sequestration which grounded the squadron in April and led to multiple losses of flying currency.

[26] In March 2011, the Warhawks deployed personnel and F-16s to Aviano Air Base, Italy,[27] to form the 480th Expeditionary Fighter Squadron[28] to support Operation Odyssey Dawn, flying cover for strike aircraft.

[31][32] In April 2013, the 480th Expeditionary Fighter Squadron was activated at Kandahar Airfield, Afghanistan, for six months to support Operation Enduring Freedom.

[39] On 30 May 2014, the 480th deployed personnel and aircraft to support the detachment at Lask for two weeks, participating with Polish forces in Exercise Eagle Talon.

[41] The 480th Expeditionary Fighter Squadron was activated at Uvda Air Base in Israel between 3 and 14 November 2019 to participate in Israeli Exercise Blue Flag 2019.

[42] On 25 October 2024, amid rising tensions in the 2024 Iran–Israel conflict, CENTCOM announced that they were deploying F-16 fighters from the 480th to the Middle East.

[43][44] On 29 July 2020, the Department of Defense announced that the 480th would be moved from Spangdahlem to Aviano Air Base, Italy as part of a plan to withdraw forces from Germany.