In 1890, the Scientific and Industrial Museum was founded in Perm, which established an art department in 1902. By 1907, this department already housed works by the professor of the Academy of Arts, historical painter Vasily Vereshchagin, and his brother Pyotr, which were gifted to their native Perm. The collection also included works by famous Russian artists such as Nikolai Gushchin and brothers Alexander and Pavel Svedomskiy. This became the foundation for the collections of the future Art Museum, which opened on November 7, 1922.

The main part of the museum's collection was gathered thanks to its founders, researchers of the cultural history of the Perm region, Alexander Syropyatov and Nikolai Serebrennikov.

In the 1920s, the museum's collection was replenished through the State Museum Fund, created as a result of the nationalization of private collections and the disbanding of many Moscow museums. During the Great Patriotic War, the collections of the State Russian Museum were stored in the gallery building, and a workshop for creating propaganda posters operated under the direction of director Nikolai Serebrennikov. Many of these posters became part of the museum's collection.

The museum's fund was also regularly supplemented through expeditions, which collected items of folk art from the Perm region, such as folk icons, costumes, ceramics, weaving, wood painting, and wooden sculpture.

The collections of the Perm State Art Gallery number about 50,000 items. They feature works of domestic and Western European art from various artistic schools, styles, and movements of the 15th to 20th centuries. The gallery pays great attention to educational and outreach activities, implementing new author programs and working with people with disabilities.

The building of the Cathedral of the Transfiguration of the Savior, which has housed the gallery since 1932, is a monument of 19th-century architecture. It is a rare case where a cathedral building has been used for so long by a non-religious organization. In December 2011, the Federal Property Management Agency for the Perm region signed an order to transfer the Cathedral of the Transfiguration of the Savior to the ownership of the Perm Diocese of the Russian Orthodox Church. By mutual agreement, the art gallery committed to vacate the cathedral building by 2016, temporarily relocating all its museum exhibits to a neighboring building of the former rocket school.