Originally known as Mosquito Bay in 1927, the airstrip was the only facility which served the island of St. Thomas. The facility was named after a nearby grassy swamp, which was renamed to Lindbergh Bay after Charles Lindbergh used it to land the Spirit of St. Louis. The first passengers landed in 1928, and the airstrip remained in civilian use until it was purchased by the US government on 1 September, 1935. The airstrip was renamed Bourne Field, after the first person to fly non-stop from the United States to Nicaragua. The field was composed of two 1,600 feet (490 m) long unpaved runways used to train aviators of the US Marine Corps. In 1940, the US Navy ordered a major expansion of the base, which saw the extension and paving of the runways along with construction work to accommodate a VMS-3 observation squadron. Once World War II began, VMS-3 patrolled the surrounding areas for enemy submarines, operating the J2F-A Duck, Vought SU-2 Corsair, OS2N-1 Kingfisher, and Douglas SBD Dauntless. By 1944, enemy submarine activity decreased. This left the base redundant, and was handed over to civilian authorities to operate in 1946.

Following the closure of the Marine base, the airport was leased to the US Department of the Interior for civilian use. However, the Navy reserved the power to reactivate the airport for military purposes. After the transfer, the former hangar was converted into the civilian terminal and named after President Harry S. Truman. The airport was eventually renamed for former governor Cyril King in 1984.

On 25 March 1950 the Department of the Interior leased the land to the Virgin Islands. However, the department canceled the lease on 1 July 1954 citing violations of the agreement. According to the department, the Virgin Islands failed to register and report financial transactions relating to the land. As a result of the cancelation, the property was given to the US Virgin Islands Corporation.

Historically, a number of airlines operated scheduled passenger jet service into St. Thomas in the past. These air carriers included Air Florida with Douglas DC-9-10s, Caribair with McDonnell Douglas DC-9-30s, Eastern Airlines with Boeing 727-100s, 727-200s and 757-200s, Midway Airlines with Boeing 737-200s and McDonnell Douglas MD-87s, Pan American World Airways (Pan Am) with Boeing 727-100s and 727-200s as well as wide body Airbus A300B4s and Airbus A310s, and Trans Caribbean Airways with Boeing 727-200s. Trans Caribbean, Pan Am and Caribair were all operating jet service into St. Thomas by the late 1960s with the airport runway only being 4,658 feet (1,420 m) in length at the time.

One air carrier that has served St. Thomas for many years is American Airlines, which began serving St. Thomas in 1970 following its acquisition of and merger with Trans Caribbean Airways. In 1975, American as well as Eastern and Pan Am were serving the airport with Boeing 727-100 jetliners, American and Pan Am with nonstop 727 flights from New York Kennedy Airport with American also operating direct one stop 727 service from Boston and Providence, RI, and Eastern with nonstop 727 flights from Miami and San Juan as well as direct 727 flights from Chicago O'Hare Airport, Cleveland and Dallas/Fort Worth.

By 1994, American was operating wide body Airbus A300-600R jets into St. Thomas with nonstop service from Miami and San Juan with direct one stop A300 flights from Chicago O'Hare Airport, Orlando and Philadelphia and was also flying nonstop Boeing 757-200 service from New York Kennedy Airport. Other airlines operating jet service into St. Thomas at this same time in 1994 included Continental Airlines with nonstop Boeing 727-200 service from New York Newark Airport, Delta Air Lines with nonstop Boeing 757-200 service from Atlanta and St. Croix as well as direct one stop 757 service from Washington Reagan National Airport, Private Jet Expeditions (operating as National Airlines at this time) with nonstops from Atlanta and direct one stop service from Chicago Midway Airport flown with McDonnell Douglas MD-80s, and USAir with nonstops from Baltimore and direct one stop service from Pittsburgh flown with Boeing 727-200s.

Historically the airport hosted Air Force One and Two, respectively, carrying Bill Clinton, Al Gore, and Joe Biden using Boeing 707s and later Boeing 757s.

Cyril E. King Airport also hosted a number of charter jet airliners including the Boeing 757, Boeing 767 and the McDonnell Douglas DC-10. A new passenger terminal opened in November 1990.