In November 1961, a public museum was established in Belomorsk. In the early years of its existence, until 1966, when the museum became the Belomorsk branch of the Karelian State Historical Museum, items and documents were received from private individuals as well as from groups of enterprises and organizations in the Belomorsk district.

Since 1966, the museum has begun to showcase unique complexes of petroglyphs, such as the rock carvings 'Devil's Tracks' and 'Zalavruga'. The archaeological collection of the museum includes items found as a result of excavations in the lower reaches of the Vyga River, at the sites of Erpin Pudas, Devil's Tracks, Zalavruga, and Gorely Bridge. These include stone axes, knives, arrowheads and spearheads, scrapers, grinding stones, and other artifacts. The museum also houses items of Pomor culture, economy, and everyday life, as well as materials on the history of the region. Among them are documents, photographs, and personal belongings of Belomorsk residents, heroes of the Great Patriotic War, teachers, athletes, and Honorary Citizens of Belomorsk. The museum holds over 5,000 items in total.

In 2008, after moving to a new building, an exhibition hall was opened, where, in addition to the main exhibition, 10-12 thematic exhibitions are organized annually. Recent exhibitions include 'Canal of Sorrow and Grief', dedicated to the 75th anniversary of the construction of the Belomor-Baltic Canal, 'Golden Patterns of Pomorye', 'Pomor Storyteller F. I. Bykov', 'From the Intercession to the Baptism', and 'Pomor Tea Party'.

The main exhibition 'Marine Culture of the Pomors at the End of the 19th and Beginning of the 20th Century' tells about traditional Pomor crafts and their historical development. It features photographs, documents, ship models, authentic fishing tools and their models, as well as household items from Pomor villages of that time.

The exhibition includes sections: 'Navigator Schools of Pomorye', 'Centers of the Pomor Coast', 'Shipbuilding' with types of ships, models, the ritual of laying a ship, and shipbuilders' tools, 'Fur and Fish Industries', 'Trade Relations' with a map of Pomor trade routes. Here, one can learn about the intricacies of herring fishing, salmon catching, methods of harvesting and processing river pearls, and much more related to the marine culture of the Pomors. Among the museum's rarities are 'Plan of the Shizhen Village from 1852' and navigational equipment. The exhibition serves as a basis for thematic tours and lectures, such as 'History of the Pomor Costume', 'Pomor Family', 'Shipbuilding in Pomorye', 'Trade Relations between Pomorye and Norway', 'Geographical Discoveries in the Russian North', and others.