The origins of the museum go back to 1940 when the village of Monino was selected to be the location of what is now the Gagarin Air Force Academy. The museum itself was founded in 1958, two years after the airfield was closed, and had 6 aircraft and 20 aircraft guns at the time. When it opened to the public another two years later in 1960, it had 14 aircraft. By early 1970, the museum's collection had expanded to about 40 aircraft. In 1990, the aircraft on display were rearranged according to design bureau and chronological order.[1] The museum's main hall with the awards, documents, uniforms and personal belongings of the famous pilots was mostly destroyed by fire in 2005.[2] By 2013, a new hangar had been built to house the World War II aircraft.[3] In 2016, it was reported that the museum was to close, with the exhibits being transferred to Patriot Park.[4] When transporting large-sized unique aircraft, the exhibits were threatened with the breakage. At the request of the Ministry of Culture, the movement was stopped. New halls with the modern equipment for exhibitions were built. However, a new exhibition hall was opened in February 2020.[5]

Prior to 1999, the museum was closed to the public, because of the display of classified prototypes from the era of the former Soviet Union.[citation needed]. Today, the museum contains a range of aircraft, both domestic and foreign, including military, civil and special purpose. The museum also houses associated pieces, such as the uniforms, documents, models and equipment related to the aircraft. The museum is currently open to members of the public to visit.[6]