When the pre-war airport, a flying boat facility on Darrell's Island, closed in 1948, Bermuda's air routes were taken over by land planes operating through the airfield.

In 1970, the field was transferred to the United States Navy, which operated it as US Naval Air Station, Bermuda until 1995.

This involved changes to the airfield lighting, erecting new fences, levelling anything over a certain height and within a certain distance of the runway (including the former base commander's residence, and the hill it stood on), and other changes.

[7] On 16 March 2017, the Government of Bermuda signed an agreement with the Canadian Commercial Corporation, granting Skyport a 30-year concession to manage and operate the airport.

It has received high marks in passenger satisfaction surveys, placing first among North American airports in the "Under 15 million passengers" category in 2003 and fourth worldwide in its size category, according to the global airport monitor report that year.

Because of Bermuda's considerable distance from the nearest land mass, the airport's use by General Aviation aircraft is limited to jets and long-range turboprops.

Air traffic control service is provided by CI2 Aviation under contract to Bermuda Skyport Corporation.

Approach, departure and en route traffic control in the surrounding Oceanic Sector is provided by New York Air Route Traffic Control Center (ZNY), under an agreement between the US Government's Federal Aviation Administration and the United Kingdom.

Remote radio transmitters and air traffic radar coverage at the airport also link Bermuda and New York Center.

Navaids at the airport, such as the Instrument Landing System (ILS) and VOR (VHF omnidirectional range), are owned by Skyport but maintained by CI2 Aviation.

The airport was a United States government NASA Space Shuttle launch abort site.