In November 1961, a public museum was established in Belomorsk. Its creation began with the decision of the Executive Committee of the Belomorsk District Council of Workers' Deputies on November 2, 1961, to open a Historical and Local History Museum in the city. In the early years, until 1966, when the Belomorsk branch of the Karelia State Historical Museum was organized based on the public museum, items and documents were collected from residents, enterprises, and organizations of the Belomorsk district.

Since 1966, the museum has started to display unique complexes of petroglyphs and rock images, such as 'Devil's Tracks' and 'Zalavruga'. The archaeological collection of the museum includes items found during excavations in the lower reaches of the Vyga River, at the sites of Erpin Pudas, Devil's Tracks, Zalavruga, and Gorely Bridge: stone axes, knives, arrowheads and spearheads, scrapers, grinding stones, and other artifacts. The museum also houses collections of items from Pomor culture, economy, and everyday life, as well as materials on the history of the region, including documents, photographs, personal belongings of Belomorsk residents, heroes of the Great Patriotic War, teachers, athletes, and honorary citizens of the city, totaling over five thousand storage units.

In 2008, after moving to a new building, an exhibition hall was opened, where, alongside the main exhibition, 10-12 thematic exhibitions are organized annually.

The main exhibition 'Marine Culture of the Pomors of the Late 19th and Early 20th Century' is dedicated to traditional Pomor crafts, their historical formation, and development. The exhibition features photographs, documents, ship models, original fishing tools and their models, as well as household items from Pomor villages of the late 19th and early 20th centuries. Sections of the exhibition include 'Navigator Schools of Pomorye', 'Centers of the Pomor Coast', 'Shipbuilding', types of ships, models, the ritual of laying a ship, shipbuilders' tools, 'Fur and Fish Industries', 'Trade Relations', and a map of Pomor trade routes. Here, one can learn about the intricacies of herring fishing, the peculiarities of salmon catching, methods of extracting and processing river pearls, and much more that constitutes the concept of 'marine culture of the Pomors'. Visitors can see one of the museum's rarities, 'Plan of the Shizhen Village from 1852' with a list of names and surnames of all homeowners, as well as navigational and surveying equipment, including 'dry' compasses. The exhibition 'Marine Culture of the Pomors' hosts 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 many others.