The first proposal to build and manage an airport in the Marche region by a local authority emerged in 1929, initiated by the Province of Ancona. It was through the Province's efforts that the history of Ancona Airport began, constructed with authorisation from the Ministry of Aeronautics in the Contrada Fiumesino area of Falconara. Initially designated as a military emergency landing field for aircraft forced to make an unscheduled descent, the airfield was developed at a cost of 2,000,000 lire for the Province. In 1933, the ownership of the land was transferred to the state. Then, in 1939, Falconara received its first official recognition when it was formally registered on the national list of civil airports.

During World War II, the airport was damaged and later occupied by the Allies, who established a NATO base there in 1950. The military presence significantly delayed efforts to restore the airport. In 1960, the Province, along with other local authorities, launched a promotional initiative to enhance airport infrastructure and encourage air travel. As a result, the first regular biweekly flights to Rome, Pescara, and Milan were introduced in 1963, followed by connections to Bari and Venice in 1964.

In 1965, with an investment of 67,000,000 lire, the involved authorities constructed a new terminal building equipped with offices and essential services. On February 5, 1968, they established Aerdorica S.r.l., tasked with promoting air traffic, managing airport services, and planning the expansion of the airport to meet the growing demands of civil air transport. The company developed the airport’s master plan and acquired the land designated as the foundation for the new civil airport. Construction began in 1977, leading to the inauguration of Raffaello Sanzio Airport near Castelferretti on July 16, 1981.

A major modernisation project was completed in June 2004 with the inauguration of the new terminal, designed by Volkwin Marg, a member of Gerkan, Marg and Partners.

Since June 2021, Ancona International Airport S.p.A. has taken over the management of the airport from Aerdorica. Alongside this transition, the airport was officially renamed Ancona International Airport – Raffaello Sanzio.