The museum-reserve was founded in 2000 by the decision of the Sverdlovsk region government. It is the successor of the Verkhoturye Local History Museum, which was opened in 1921, disbanded in the mid-1930s, and recreated in 1977. The museum-reserve's collections include those from the local history museum, as well as a number of cultural heritage sites of federal and regional significance.

The museum is located in the historical center of Verkhoturye and includes the Verkhoturye Kremlin on the Trinity Stone above the Tura River, as well as the House for Receiving Honored Guests on the left bank of the Kalachik River, a tributary of the Tura.

The uniqueness of the Verkhoturye Museum-Reserve lies in the fact that it is the only museum in the Sverdlovsk region located on the territory of an 18th-century stone kremlin, which serves as a cultural, historical, religious, and public center of the city. The ensemble of the Verkhoturye Kremlin includes cultural heritage sites from the late 17th to early 20th centuries, such as the Holy Trinity Cathedral, the Tsar's Granaries, the Voivode's House, the Order Chambers, and the County Treasury. It also houses archaeological monuments and a number of restored objects, including the Kitchen and Guardhouse, the Storage Chambers, the Gunpowder Cellar, and fortress towers.

The total area of the museum-reserve is 3.4 hectares.

It is visited by more than 50,000 people annually.