Originally opened as an RAF base, it came under government ownership in the 1960s before being sold to Haughey Airports in 2000 which was later purchased and rebranded as Stobart Air Limited.

Since its partial re-opening post COVID-19, it now operates unlicensed and welcomes general aviation aircraft, as well as being host to several military exercises throughout the year.

With the outbreak of war in 1939, RAF Kingstown's runway was too small for bombers, so the Royal Air Force developed a new airstrip at Crosby-on-Eden to the east of Carlisle, on the line of the Stanegate Roman road.

After a short refurbishment programme it was licensed in 1961 for training purposes and civilian flights to destinations including London, the Channel Islands, Belfast and the Isle of Man.

The trainee pilots had a reputation locally for being slightly reckless with various incidents occurring during the period that Specialist Flight Training were operational at the airport.

Haughey invested £4 million in infrastructure improvements but, whilst promising to provide additional facilities and enhancements to the site for the Solway Aviation Museum, he sold the airfield to WA Developments Limited in 2006 before achieving this.

Following an independent shareholder vote, the acquisition was completed on 30 May 2009, and the purchase price was reduced to £9.9 million due to a fall in the value of Stobart Group shares.

Between December 2014 and September 2015, a £12 million freight distribution centre was built on the south-eastern corner of the site, which is now leased to Eddie Stobart Logistics.

After financial assistance from the Cumbria Local Enterprise Partnership, there were plans for passenger flights from June 2018 "to major tourism and business hubs including London, Dublin and Belfast" but the target date was postponed.

[14][15] Plans were announced to redevelop the airport site to include a new passenger terminal, an air freight service, a new headquarters for Eddie Stobart, and a 750,000-square-foot (70,000 m2) distribution centre.

Following a change in the law which no longer required Stobart Air to prove that the airport would have to be viable, planning permission was re-granted on 18 August 2014.

This first development covers 19 acres, and this site was sold to the real estate investment fund Gramercy Europe for £16.925 million on 22 February 2016.

[29] On 22 November 2016, Stobart Group announced it was developing 21 acres of land adjacent to its existing Air Freight Distribution Centre in an area to be called Eden Park.

[31] Start-up airline Lakeland Airways attempted to establish flights from Carlisle in 2021, but later moved its base to Blackpool following the revocation of the airport's commercial licence.

Although not present during the COVID-19 pandemic between 2020 and 2022, the Royal Netherlands Air Force has been holding their annual low flying exercise "Tac Blaze" over the nearby RAF Spadeadam range while based at the airport since 2006.