The Museum of the History of Yaroslavl was opened in August 1985 as a branch of the Yaroslavl State Museum-Reserve. Since 1998, it has become an independent municipal museum.

The museum is located in a merchant's estate on the Volga embankment. The main building of the estate was constructed in 1893-1894 with funds from merchant of the 1st guild Vasily Yakovlevich Kuznetsov, whose fortune was estimated at nearly 1 million rubles by the end of his life. After his death in 1901, the house passed to his widow, Elizabeth Maximovna Kuznetsova. In 1918, the building was nationalized and used for various institutions, including a children's hospital and an eye department.

In 1985, the house became the Museum of the History of the City. In 1998, thanks to the initiative of the mayor and the support of the governor, the museum became municipal, which was related to the preparations for the 1000th anniversary of Yaroslavl. The museum was headed by Vladimir Georgievich Izvekov, under whose leadership renovation and restoration work was carried out and a new exhibition was created. The project was funded by the city budget and sponsorship from more than 40 organizations, which were noted in the Museum's Book of Friends. The restoration of the building was carried out by architects-restorers S. N. Stolyarova and S. E. Novikov.

The museum's exhibition, "Ten Centuries of Yaroslavl's History," covers the entire history of the city from the 11th century to the present day. It includes six thematic halls, featuring archaeological finds, monuments of writing, and other exhibits. Special attention is given to a model of Yaroslavl from the 13th century. The exhibition also covers the period of the Moscow Tsardom, the Time of Troubles, and the development of the city in the 18th century, including the Yaroslavl Great Manufactory and the creation of the province.

The fifth hall is dedicated to the political history of the city, including events of the First Russian Revolution and World War I, as well as the Yaroslavl uprising of 1918. The sixth hall covers the second half of the 20th century and the modern history of the city. The museum also includes halls dedicated to famous Yaroslavl residents and the city's international relations.

In 2002, the exhibition "From the History of Yaroslavl Medicine" was opened, and in 2016, "World Heritage Monument," dedicated to the historical part of Yaroslavl included in the UNESCO list. The museum has two branches: the City Exhibition Hall named after N. A. Nuzhin and the Center for Belarusian Culture. From 2012 to 2019, the museum was headed by Valery Vasilievich Velichko, and since May 2019, the director has been Alexander Vitalievich Nechaev.