The Ulyanovsk Puppet Theater was founded on April 1, 1944, under the guidance of artists from the Moscow operetta N.V. and M.N. Misyura. In 1945, it became professional, and in 1948, it began its season in the building of the House of Teachers, where the Ministry of Arts and Cultural Policy of the Ulyanovsk Region is currently located. The theater's first production was "The Goat and the Kids." In 1970, the theater moved to a 19th-century architectural monument, where it remains to this day.

In June 1999, reconstruction began: the courtyard part, which made up 2/3 of the building, was demolished, leaving only the facade. In December 2000, the theater celebrated its new home. For the theater's 60th anniversary in 2004, the need for new repairs arose, which were carried out in 2005 with funds from a private benefactor.

On July 17, 2007, the theater was named after the People's Artist of the USSR V.M. Leontyeva. A memorial corner was created in the theater museum, where among the exhibits is a unique audio disc with the voice of V.M. Leontyeva and copies of puppets from the show "Good Night, Little Ones!" made in the theater's workshops. In April 2008, a monument to V.M. Leontyeva was installed opposite the theater.

In 2008, with the support of the Government of the Ulyanovsk Region and the Department of Culture and Archive Affairs, the Ulyanovsk Puppet Theater established the first interregional puppet theater festival "Puppet Format 2008," which featured theaters from the Volga Federal District.

The theatrical museum, opened in 1991, houses a unique exhibition, including a multi-figure composition by master Alexei Antonovich Morozov, created in 1905. It features 60 miniature dolls depicting peasant life of that time, each playing its role. The composition represents a model of the author's native village. The figures are made of beech, ash, alder, and cherry and have been preserved in perfect condition. For over 110 years, the collection has amazed audiences. The museum also showcases theatrical puppets of various systems, posters, and awards of the theater.