The first building specifically designed for the theatre was erected in 1846. It was wooden and primarily used for the tours of traveling theatre companies, such as P. A. Sokolov's troupe. The new city theatre opened on November 24, 1870, with M. I. Glinka's opera "A Life for the Tsar" as its first production. The construction of the stone theatre building was completed in February 1880. In 1926, a permanent ballet troupe was established. In 1965, the theatre was named after P. I. Tchaikovsky, and in 1969 it received the status of an academic theatre. During the Great Patriotic War, the Leningrad State Academic Theatre of Opera and Ballet named after S. M. Kirov (now Mariinsky Theatre) was evacuated to the Urals, significantly influencing the development of the Perm theatre, especially ballet. Artists and teachers from the Kirov Theatre helped establish a choreographic school in the city, which is now the third most significant in Russia.

For the 200th anniversary of A. S. Pushkin's birth, the theatre presented the project "Opera Pushkiniana," which includes five operas based on the poet's works. The directors were awarded the State Prize of the Russian Federation for 1999. The theatre collaborates with renowned scenographers such as Y. Ustinov, I. Akimova, V. Okunev, Y. Kharikov, and A. Kozhenkova. Joint projects continue with the George Balanchine Foundation. In 2004, the opera troupe participated in the contemporary art festival "Sacro Art" in Loccum (Germany) with A. Shchetinsky's "Bestiary." The ballet troupe presented Tchaikovsky's "Swan Lake" in Munich and Antwerp. The theatre's ballet troupe is considered one of the most famous in Russia and successfully tours abroad under the brand "Tchaikovsky Ballet." In 2018, the dramatic oratorio "Joan of Arc at the Stake" by Arthur Honegger received the Russian opera award CASTA DIVA in the "Event of the Year" category and won in the "Opera/Performance" category of the Golden Mask theatre award.