The new Vatican Pinacoteca was opened on 27 October 1932 in the building especially constructed by the architect Luca Beltrami for Pius XI. It was built in the nineteenth century Square Garden, isolated and completely surrounded by avenues, in a place considered suitable for assuring the best lighting conditions for both the correct preservation of the works and their optimum aesthetic enhancement.

Thus the age-old question of the exhibition of the paintings, which were constantly moved around the Apostolic Palaces due to the lack of a setting that matched their importance, was solved. A first collection of only 118 precious paintings was created by Pope Pius VI around 1790. It was of short duration due to the fact that, following the Treaty of Tolentino (1797) some of the greatest masterpieces were transferred to Paris.

The idea of an art gallery, understood in the modern sense as an exhibition open to the public, was only born in 1817 after the fall of Napoleon and the consequent return to the Church State of a large part of the works belonging to it, according to the directions of the Congress of Vienna.

The collection continued to grow over the years through donations and purchases until it reached the current nucleus of 460 paintings, distributed among the eighteen rooms on the basis of chronology and school, from the so-called Primitives (12th-13th century) to the 19th century.

The collection contains some masterpieces of the greatest artists of the history of Italian painting, including Giotto, Beato Angelico, Melozzo da Forlì, Perugino, Raphael, Leonardo, Tiziano, Veronese, Caravaggio and Crespi.