On 6 August 1941, construction began on the future site of Marine Corps Air Station at Cherry Point, North Carolina. The air station was finally completed on 20 May 1942, becoming the largest air stations operated by the Marine Corps with over 17 square miles of area.
Originally, the predecessor of the present Headquarters and Headquarters Squadron was activated as Cunningham Field, Cherry Point during August 1941. A few months later, on 1 December 1941, it was redesignated as Headquarters Squadron, U.S. Marine Corps Air Station, Cherry Point. From the beginning of World War II to the present, it has functioned as the administrative unit for the commanding general of the air station and his staff. Since its activation, the air station's mission has been that of maintaining and operating facilities and providing "services and material to support forces of the Navy and other activities and units, as designated by the Chief of Naval Operations".
On 25 February 1954, Headquarters squadron for the base was redesignated to its present designation of Headquarters and Headquarters Squadron, Marine Corps Air Station, Cherry Point.
During the period 1 July 1985 to 31 October 1986, the squadron was presented a Meritorious Unit Commendation for meritorious service in the areas of administrative, operational, and logistical support for Marine Corps Air Station, Cherry Point, North Carolina and all Second Marine Aircraft Wing tenant commands.