The airfield began modestly. English Wikipedia, drawing on Slovenian local press, says the Yugoslav military authorities picked the site in the 1930s for its weather and terrain and laid a grass runway as an auxiliary field, with wooden hangars. When Germany, Italy and Hungary invaded Yugoslavia in April 1941, the Royal Yugoslav Army’s 6th Air Reconnaissance Group, attached to the 7th Army, was here. It lost nine aircraft on the first day, leaving three Breguet 19s and a Fieseler Storch.

The Germans expanded the field between the autumn of 1941 and the spring of 1942, lengthening the runway and adding three brick buildings. It was liberated on 9 May 1945. The Yugoslav People’s Army took it over and upgraded the runway in November 1953, during the Trieste crisis with Italy. By the end of the Yugoslav era the 82nd Aviation Brigade was based here, with the 237th Fighter-Bomber Squadron on J-21 Jastrebs, the 238th on J-22 Oraos and the 351st Reconnaissance Squadron on the IJ-21 and IJ-22.

Cerklje played no direct part in the air war over Slovenia in the sources checked, but its fate shows what the new state inherited. In the summer of 1991, as the Brioni Declaration ended the Ten-Day War, all Yugoslav units withdrew to Bosnia and Herzegovina and Serbia and took their equipment with them. The last Yugoslav troops left Slovenia on 26 October 1991.

Slovenia therefore gained a well-sited airfield but no aircraft to put on it. The 15th Military Aviation Brigade, named on 9 June 1992, flew from Brnik and Cerklje, and after the 2004 reorganisation Cerklje held the Air Force School and the air base while the helicopters stayed at Brnik.

On 7 December 2006 the defence minister, Karl Erjavec, and three ministerial colleagues signed a protocol on reconstructing and developing the airfield, including facilities for transiting NATO aircraft. English Wikipedia notes that the plan worried residents across the border in Croatia over its environmental impact.

The ministry’s own summary of the work, published in March 2021, lists a new control tower, aprons, runway lighting to CAT I, navigation and weather equipment, hangars, a technical building, a fuel storage complex, warehouses and a fire and rescue station, plus water, power and a bypass road. The first phase cost €72.5 million (€41 million NATO) and the second €33.2 million (€31 million NATO). About 70 per cent of the work went to Slovenian contractors, and the ministry paid over €5 million into the local community. The stated goal was ILS operations and aircraft up to code 4E.

Cerklje is now the base of the 15th Military Aviation and Air Defence Brigade, formed in May 2024. The C-27J Spartan Martin Krpan arrived on 19 December 2023 and was received the next day by the defence minister, Marjan Šarec, and the regiment’s commander, Colonel Janez Gaube; because there was no hangar large enough, it was parked at Maribor at first. The second Spartan, Edvard Rusjan, followed on 17 December 2024.

In June 2025 the base opened its gates for the 12th Adriatic Strike exercise, with about 800 participants from 30 allied and partner nations, seven helicopter types from four countries and nine fixed-wing types from nine. The medium-term defence programme adopted in November 2025 names the further development of Cerklje as a priority, and the brigade expects new airfield systems to be installed in 2026.