The Historical Museum is part of the Smolensk State Museum-Reserve and is considered the oldest in its structure. In 1888, local historian S.P. Pisarev opened a historical and archaeological museum in the building of the City Duma. Since then, the collections have significantly expanded, the museum has changed its name and location, but continues to introduce visitors to the rich history of the Smolensk region.

The museum is actively working on creating a permanent exhibition. Sections such as "The Earliest History of Smolensk Land" (100,000 years ago, early IX century AD) and "Smolensk in the Ancient Russian State in the IX and early XIII centuries" have already been opened. The exhibition "The Earliest History of Smolensk Land" features over 1,500 items from the archaeological fund that illustrate the history of the region from the Stone Age to the early Middle Ages. Among the exhibits, one can see flint tools, stone axes, fragments of clay vessels, bronze jewelry and cult objects, as well as models, maps, and reconstructions. A genuine mammoth skeleton occupies a special place.

In the second hall of the permanent exhibition, unique archaeological finds from the Gnezdovo complex (IX-X centuries) are presented: a jug-amphora with the oldest Russian inscription, Frankish steel swords, gold coins of Byzantine emperors Alexander and Theophilus, silver Arab dirhams, bronze and brass jewelry, fibulas, and buckles. One can also see reconstructed appearances of the inhabitants of the Gnezdovo settlement and their costumes.

The museum showcases unique archaeological monuments of ancient Smolensk (XI-XIII centuries): the seal of Prince Vyacheslav Yaroslavich, the stone tomb of Prince Davyd Rostislavich, birch bark letters, weapons of Russian knights, frescoes from temples, silver grivnas and ingots, Western European denarii, tools, and crafts. There are also household items of ancient Smolyans, a fragment of an 800-year-old house, and models of temples. The exhibition is accompanied by maps, reconstruction drawings, schemes, plans, and explanatory texts.

In 2014, a new section of the exhibition "History and Culture of Smolensk Region in the XIII-XVIII Centuries" was opened. It reflects key moments in the region's history: the Mongol-Tatar invasion, relations with the Grand Duchy of Lithuania, the return of Smolensk to the Russian state in 1514, the construction of the fortress wall, defense against Polish invaders, liberation in 1654, the reforms of Peter I, participation in the Northern War, and the development of the Smolensk province.

The new exhibition features over two thousand exhibits, many of which are displayed for the first time, showcasing more than 500 years of the region's history.

In 2017, the fifth hall of the exhibition was opened, dedicated to the Smolensk province in the first half of the XIX century: events on the eve of the Napoleonic invasion, the Patriotic War of 1812, the participation of Smolyans in the Decembrist movement, the socio-economic development of the region, and the flourishing of Russian culture.