The history of the Irbit Historical and Ethnographic Museum began in 1883 when, with the support of the Irbit Zemstvo, a traveling pedagogical museum was opened at the county's three-class school. The inspector of the school and member of the UOLE, Semyon Vasilyevich Fedoseev, participated in its creation. Until July 1905, the museum functioned as a school museum, and then it became public. In 1911, the widow of a first-guild merchant and the mayor of Tomsk, P. V. Mikhailov, Alevtina Petrovna, donated her husband's house to the city, located near the Sretenskaya Church on Konstantinovskaya Street, 1. The city council decided to place a women's primary school in it, and in the annex, a museum and library.

During the Civil War, Irbit experienced looting and fires, resulting in the loss or destruction of many museum exhibits. In February 1921, the museum began its activities under new conditions. At the initiative of the education department of the Irbit Political Education, it was transformed into a teaching and demonstration museum of visual aids for the county department of public education, with 3,675 exhibits. The restoration of the museum was overseen by Andrey Prokopyevich Solovyov, who worked in various positions until 1948. In the early 1930s, thanks to the efforts of M. D. Golubyh, the museum moved to a new building and actively expanded its collections. In 1941, the museum was closed and did not operate, but in 1943 it reopened at 50 Kirova Street, where it is still located today.

After the war, the museum staff actively worked on replenishing its collections. In 1979, the institution received the status of a historical and ethnographic museum. In 2009, a second building of the museum opened at 74 Kirova Street. During its operation, the museum has been visited by over 2 million people.

As of 2017, the museum had 14,157 exhibits in its main collection and 8,690 in its auxiliary collection, and their numbers continue to grow.