The public museum in Kargopol was founded in 1919. Its creator and first director was the Kargopol merchant Kapiton Grigoryevich Kolpakov (1845, 1922), whose collection served as the foundation for the museum's collection. His collection included ethnographic exhibits, manuscripts, weapons, portrait paintings, and porcelain.

On March 27, 1919, an agreement was signed for the transfer of a collection of nearly 600 items from K.G. Kolpakov to the district department of public education, marking the founding date of the museum in Kargopol. Initially, the museum was housed in Kapiton Grigoryevich's home.

In 1923, the museum was given the building of the Cross Exaltation Church, which no longer exists, and it opened to the public for the first time. In 1933, the museum was transferred another church building, the Introduction Church. In the 1920s, the museum received icons, books, church utensils from closing churches and monasteries, as well as items from wealthy families. They were stored in the Nativity Cathedral, which was transferred to the museum in 1936.

Until the early 1980s, the museum had a single exhibition hall in the Introduction Church, where a local history exhibition was displayed. In the early 1980s, the church of Saints Zosima and Savvatiy was transferred to the museum, and soon the Trinity Church joined its collection. In 1993, architectural ensembles in the villages of Lyadiny, Oshevensk, and Saunino were transferred to the museum. From 1994 to 1996, the church of John the Baptist was part of the museum, later returned to the diocese. In 1995 and 2004, historical buildings of civil architecture were added to the museum: the house of merchant Blokhin and the house of timber industrialist Vager.

Currently, the museum's funds contain over 48,000 storage units, of which 33,000 are the main collection. Folk costumes, Kargopol embroidery, gold sewing, wood painting, handwritten and old printed books, church sculpture, and icon painting make up the museum's best collections. The collections of handwritten and old printed books, as well as the cartographic collection, are of scientific interest.

The museum regularly hosts exhibitions dedicated to ancient Russian and folk art, as well as historical and children's exhibitions. The collection of Kargopol women's costumes from the 19th and early 20th centuries forms the basis of the traveling exhibition "The Warmth of a Woman's Soul." The museum oversees numerous cultural projects.

The exhibition halls of the museum are located in buildings of cult architecture: the Nativity Cathedral, the Introduction Church, and the church of Zosima and Savvatiy. In July 2009, a two-story civil building was transferred to the museum, where a Museum and Exhibition Center was created. Here is the Library of the Russian North named after G.P. Gunna, as well as exhibitions and displays representing the museum's collections and traveling exhibitions.