The Exhibitions Office was established as an independent service in 1997 with the aim of handling two distinct types of activities. On the one hand, it deals with the day-to-day management of loans of works of art from the Vatican Museums to temporary exhibitions around the world and, on the other, with the organisation of exhibitions featuring works from the Museums in the Vatican or abroad.

The management of loans involves continuous dialogue with external parties (requesting institutions and museums, insurance companies, transport and packaging companies, customs, etc.) and internal parties within the Vatican or the Museums themselves (Legal Office, restorers, curators, conservators, logistics, administration, archives, photographic services, security, etc.). The Office is responsible for the overall coordination of all these activities. Exhibitions organised within the Vatican include those held in the Multipurpose Hall (until 2010) or in the Braccio di Carlo Magno (until 2019). Until a few years ago, the Office was also fully involved in the creation of numerous temporary exhibitions with works from museums in Italy and abroad (the last of which was in Moscow in 2016).

Starting in 2017, a series of small exhibitions (Museums at Work) was launched, set up in Room XVII of the Vatican Pinacoteca and now in its twenty-fifth edition. The intention is to show visitors the results of the day-to-day activities of the departments and laboratories by presenting restored works, “guest” works, new acquisitions and works in storage. These are small-scale initiatives, featuring a limited number of objects accompanied by a wealth of educational material to offer the public a less hurried, more in-depth and informed approach to the works. From 2025, also considering the success achieved, the space dedicated to these initiatives was doubled with the use of the adjacent Hall XVIII.

The Papal Palace of Castel Gandolfo Complex has launched a program of temporary exhibitions throughout its various spaces. A permanent exhibition dedicated to the reception of war refugees in 1944 has been set up, and subsequently three precious tapestries by Raphael for the Sistine Chapel have been displayed. A new area intended for thematic exhibitions has also been created, thereby expanding the exhibition offerings of this prestigious venue.