Mozes Kilangin Airport, constructed in mid-1969 and officially inaugurated in 1971, was originally built by Freeport specifically to support the operations of the giant mining company at the Grasberg Mine. At its inception, the airport was designed solely for non-commercial flights, serving as a transport hub exclusively for Freeport employees. It was not until 2013 that the airport underwent a significant shift in ownership, with a partial transfer to the Indonesian government, which allowed for the expansion of services to include commercial flights. As of 2022, negotiations are underway to fully transfer the ownership of the airport to the Indonesian government.

In spring 1974, Merpati Nusantara Airlines operating a flight from Kupang to Timika via Darwin, marking the first airport in Central Papua to gain international status.

On 18 July 2008, Minister of Transportation Jusman Syafii Djamal officiated the elevation of Mozes Kilangin Airport's status to that of an international airport, a move that was anticipated to boost regional connectivity. However, due to the lack of international flights, the airport’s international status was soon revoked. Efforts have been made by the local government to restore the airport's international status, but these have yet to materialize.

To increase the airport's capacity, two new terminals were constructed. The first terminal, Terminal A, commenced partial operations in 2021 and was fully inaugurated in 2022, replacing the old terminal. Terminal B is currently under construction and is expected to be completed by late 2025.

Due to its proximity to the Papuan highlands, Yohanis Kapiyau Air Force Base, the military airbase located at the airport is considered as a vital strategic asset for the Indonesian military. It has served as a forward operating base for various military operations against Papuan separatist groups as part of the ongoing insurgency in Papua. Notable missions launched from the base include the rescue of hostages during the Mapenduma hostage crisis in 1996 and the Nduga hostage crisis between 2023 and 2024, during which a New Zealand pilot was taken captive by separatist forces.

Despite its strategic importance, the airbase lacks several essential facilities. It is currently without a military apron, base operations center, aircraft and helicopter shelters, hangars, office buildings, and a dedicated military fuel station. Furthermore, accommodations (mess facilities) for standby operational crews remain limited.

In view of these shortcomings—and considering the increasing operational demands, the planned deployment of an air squadron, and the proposed upgrade of the base to Type B status—additional land is required to expand administrative and residential facilities. As part of these development efforts, Yohanis Kapiyau Air Force Base is set to receive a grant from the Mimika Regency Government for the construction of a new apron and taxiway.