The municipal collection of modern art in Venice is initiated in 1897 to coincide with the second edition of the Biennale. In 1902 the City of Venice designates Ca' Pesaro, a prestigious Baroque palace recently donated to the city by Duchess Felicita Bevilacqua La Masa, as the permanent home of the International Gallery of Modern Art. At the same time in the mezzanine were hosted, in the years between 1908 and 1924, the historic Bevilacqua La Masa Exhibitions, which, in lively contrast to the Venice Biennials, fostered a young generation of artists including Boccioni, Casorati, Gino Rossi, and Arturo Martini.

The collection was enriched over time through purchases and donations. For the former, these are essentially the works purchased by the City at the Venice Biennales. Until the 1950s, European art is favored. Beginning in the 1960s, a new policy of purchases turns instead to European art. This resulted in particular in increased works by the group of artists already mentioned, who with the Bevilacqua La Masa Exhibitions and the battles related to them had made Ca' Pesaro famous as a driving center of renewal in Italian art.

Donations began with the founding one in 1897 by Prince Alberto Giovanelli, followed by Baron Edoardo Franchetti, Baron Ernst Seeger, Filippo Grimani, and above all the Venetian Industrialists and Merchants Association. In 1914 the most prestigious waxworks by Medardo Rosso were acquired, in the 1960s the De Lisi bequest that enriched the Gallery with works by Morandi, De Chirico, Carrà as well as Kandisky, Mirò, Matta.

The museum is included in the network of the Fondazione Musei Civici di Venezia.