The art museum in Ryazan was founded in 1913 thanks to the initiative of local enthusiasts who created the "Society of the Ryazan Art and Historical Museum named after Professor Ivan Petrovich Pozhalostin." The Society included artists from Ryazan, such as Alexander Alexandrovich Kiselev-Kamsky, Vladimir Pavlovich Sokolov, Sergey Andreevich Pyrsin, as well as representatives of the local intelligentsia, including civil servants, doctors, and teachers. The first exhibits of the museum were donated by Moscow artists and included a collection of drawings and engravings by Professor of the Imperial Academy of Arts I. P. Pozhalostin.

In January 1915, the museum came under city management and opened its doors to visitors on March 23 of the same year. Its catalog listed 72 exhibits, among which were about fifty paintings and graphic works, many of which are still presented in the permanent exhibition of Russian art from the early 20th century. The exhibition was housed in the building of the city Romanov School on Seminar Street, where the museum was temporarily allocated a hall and two rooms. Today, this red brick building is one of the buildings of the Ryazan State University named after S. A. Yesenin.

In 1918, the museum became part of the Provincial Historical and Local Lore Museum. In 1938, the art department of this museum was transformed into the Ryazan Regional Art Museum. Initially, the museum was located in a separate two-story stone building of the Consistory from the 17th century, designed by architect Yu. K. Yarshev, on the territory of the Ryazan Kremlin.

Since 1980, the museum has been located in a monument of Russian classicism from the late 18th to early 19th century, the architect of which is unknown but is believed to belong to the circle of M. F. Kazakov. The building, which previously belonged to the Ryazan merchant Gavrila Vasilyevich Ryumin, was transferred by his son, Nikolai Gavrilovich, to the Ryazan Provincial Gymnasium for the boarding of noble children in 1833. In 1868, a two-story structure was added to the eastern side of the building for the altar part of the gymnasium church in the name of St. Nicholas, consecrated in 1869. This is now the entrance to the museum from Svoboda Street. In 1998, the museum was renamed after I. P. Pozhalostin.

The museum's permanent exhibition is supplemented by monthly exhibitions from its collections, as well as from the collections of other museums in the country. It hosts solo and group exhibitions of contemporary artists from Ryazan, Moscow, St. Petersburg, and other cities in Russia. The best works from the museum's collection are exhibited at international exhibitions.