The airport was officially opened in December 1963. It replaced Polje Airport in the former Municipality of Polje near Ljubljana, which served as the city's airport from 1933 and was Slovenia's first civil airport. Regular flights from the new airport at Brnik began in January 1964.

In the 1980s, Jat Airways offered flights from Chicago to Belgrade that included a nonstop segment between New York City and Ljubljana. The airline employed McDonnell Douglas DC-10s on the route. However, the flight from Belgrade to Chicago did not stop in Ljubljana.

On 27 June 1991, two days after Slovenia's Independence from Yugoslavia, the Yugoslav People's Army began its military operations within the country. The airport was bombed during the first day of the war. The next day, 28 June, two journalists from Austria and Germany, Nikolas Vogel and Norbert Werner, were killed from a missile that struck their car near the airport, where they were both driving by during that time. Four Adria Airways airliners also took serious damage from the Yugoslav Air Force.

The fighting ended on 7 July with the Brioni Agreement.

On 8 December 2004, the airport received its first annual millionth passenger. Overall, the airport handled 1,721,355 passengers in 2019, representing a 5% drop in traffic figures compared to the previous year.

In 2007, the right-wing government proposed renaming the airport from Aerodrom Ljubljana to Ljubljana Jože Pučnik Airport. Jože Pučnik was a Slovene right-wing public intellectual, dissident, politician, and leader of the Democratic Opposition of Slovenia (Demos) between 1989 and 1992.

Due to growing air traffic and Slovenia's EU entry, which requires the separation of traffic into Schengen and non-Schengen, Aerodrom Ljubljana Airport Authorities have prepared a redevelopment plan for the passenger terminal. The expansion was to be carried out in two phases. Works on the first phase began in early July 2007 to accommodate Slovenia's entry into the Schengen Area in December 2007. The terminal building (T1) was extended with a new upper level which added an additional 4,000 m2 (43,000 sq ft) to the departure lounge and four jetways have also been installed for easier passenger access to and from the terminal. In 2013, the second phase of terminal expansion which included a new terminal T2 was scrapped by the minority stakeholders.

In 2014, the Slovenian government initiated a privatisation process of the airport. The bid was won by Fraport which, in turn, acquired a 75.5% stake in the airport. The remaining shares were acquired in the following months resulting in Fraport taking 100% ownership of the airport.