The formation of the museum collection took place in the 1960s and 1980s, starting with numerous expeditions to various regions of the area. Thanks to the active collecting activities of the museum during those years and the work of restorers, a unique collection of the department of ancient Russian art was created, including about 5,000 works of painting, sculpture, and decorative applied art from the 14th to the 18th centuries. The main part of the collection consists of icons, known collectively as "northern letters." All exhibits represent monuments of the original culture of the Russian North.

The collection of folk art at the museum encompasses all types of traditional creativity from the Arkhangelsk North from the 18th to the 20th centuries: folk embroidery, weaving, gold embroidery, pearl and bead sewing, carving, and painting on wood. Among them are unique monuments that have survived in single copies.

The Arkhangelsk Museum has the most significant collection of contemporary Kholmogory bone carving, an art form that dates back to the 16th century. The works of contemporary masters in this collection rival the best examples of the past.

Other collections of the museum are also significant in volume and composition: the collection of Russian classical art and the collection of contemporary art, a crucial part of which consists of works by Arkhangelsk artists. The creativity of the older generation of masters, such as D. Shiryayev, D. Sveshnikov, V. Preobrazhensky, I. Kotov, and B. Lukoshkov, is most fully represented.

During its existence, the museum has increased its collections twentyfold, and now its collection numbers over 34,000 items in the main fund.

With a rich collection, the museum actively engages in exhibition, scientific research, educational, and publishing activities. More than 30 exhibitions are held annually at the museum, attracting over 100,000 visitors.

The museum's collections have been exhibited multiple times in major museums in Moscow. Among the most significant exhibitions in recent years are: "Carved Iconostases and Wooden Sculpture of the Russian North" at the Tretyakov Gallery, "Northern Letters" at the State Historical Museum, and "Golden Map of Russia. Portrait of the Museum. Searches and Discoveries" at the Tretyakov Gallery. Exhibitions from the Arkhangelsk Museum's collection are also in demand abroad and have been shown in Poland, Czechoslovakia, Belgium, Germany, Norway, Finland, England, Iceland, and Japan.

Currently, the Museum of Fine Arts features permanent exhibitions: Christian art from the 14th to the 20th centuries (painting, sculpture, decorative applied art) and folk art of the Russian North (northern Russian folk costume, Kholmogory bone carving, painting and carving on wood, weaving and embroidery, clay toys).

Since 2008, the museum has operated an information and educational center "Russian Museum: Virtual Branch," where screenings of multimedia films and interactive educational programs created by the staff of the Russian Museum based on their collections are organized.