An expansion of the airport during the War led to the discovery of the archaeological remains of a Neolithic settlement belonging to what is now called the Ronaldsway culture, in honour of this site.

RAF operations continued until 1943 when the airfield was handed over to the Admiralty for further development as a Fleet Air Arm training station.

Now a naval air station, RNAS Ronaldsway, the airport was taken out of commission in 1943 for almost twelve months of extensive development undertaken by John Laing & Son.

[5] The airport reverted to solely civilian flying almost immediately after the war, but the airfield remained in Admiralty possession until sold to the Isle of Man Government for £200,000 in 1948, far short of the £1 million that the UK Government had spent on constructing the airport buildings and runways, plus the £105,000 that was paid by the Admiralty in 1943 to purchase the site.

Several Manx-based airlines were formed in the early postwar years to operate scheduled and charter services to the UK mainland.

A project by Ellis Brown Architects began in November 1998 to extend the airport and improve the facilities available to passengers.

In March 2000 the new extension was opened, providing a new landside catering outlet, arrivals area, baggage hall, and departure lounge.

During the extension and renovation period, the iconic Three Legs of Man sculpture adorning the airport's façade was also refurbished.

In March 2006 funding for a further extension was granted by Tynwald to increase the number of departure gates, with work due for completion in summer 2007.

[6] It was part of a £44m plan which also included resurfacing of the runway during summer 2008 and the extension program that will commence in spring 2008 work was completed by early 2011.

[7] There has been a significant overspend on the project due to poor foreign exchange management of the Euro-denominated components of the costs.