The squadron was first activated in 1942 as the 324th Bombardment Squadron. After training in the United States, it deployed to the European Theater of Operations, where it participated in combat from late 1942 until V-E Day, earning two Distinguished Unit Citations. Following the end of the war, it returned to the United States and was inactivated in November 1945.
The unit was activated as the 324th Reconnaissance Squadron under Strategic Air Command in 1947. The following year it moved to McGuire Air Force Base and began to equip with bombers modified for long range reconnaissance. It continued in the strategic reconnaissance role until 1957, when it was inactivated.
In 2009, the squadron was converted to provisional status as the 324th Expeditionary Reconnaissance Squadron and assigned to United States Air Forces Europe to activate or inactivate as needed.