St. Peter and Paul Cathedral is located on an elevation that descends to the floodplain of the Ushayka River. This area has been known since the 17th century as "Mukhin Hill," named after the bandit Mukha, who was notorious in the surrounding forests in the late 17th and early 18th centuries. Before the construction of the church, there was a wooden cross and a chapel for a long time.

The church was built in the early 20th century according to the design of architect A. I. Langer in the neo-Russian style. The main altar, dedicated to the apostles Peter and Paul, was consecrated in 1911. The southern chapel, dedicated to St. John the Baptist, was consecrated in 1913, and the northern chapel, in honor of the Nativity of the Blessed Virgin Mary, in 1915. Services ceased in 1938, and in 1940, storage facilities for a distillery were placed here. Services resumed in 1945. In the 1950s and 1990s, St. Peter and Paul Cathedral and the Holy Trinity Church remained the only functioning Orthodox churches in Tomsk.

The building's distinctive feature lies in its decor and detailing, made of red facing brick and yellow sandstone. The facade is adorned with terracotta tiles.

Today, a Sunday school, a youth club, and a library operate at St. Peter and Paul Cathedral.

The main relics of the church include a reliquary cross with particles of the relics of 24 saints and soil from Ephesus from the grave of the apostle and evangelist John the Theologian.

The church's icon collection includes an icon of the Holy Apostles Peter and Paul with particles of their relics and an icon of the Sign of the Mother of God, created by Tomsk icon painters I. Pankryshev and S. Vepryev. Specifically for the consecration of the cathedral, four icons on cypress boards were brought from Athos to Tomsk: "The Entry into the Temple of the Most Holy Theotokos," "The Nativity of Christ," "The Beheading of St. John the Baptist," and "The Protection of the Most Holy Theotokos," created by Athonite monk-icon painters.

A miraculous icon is the image of St. Nicholas of Myra, which survived a nighttime fire during the Epiphany celebrations in 1986. The fire extinguished itself, reaching the icon without human intervention. Signs of the fire are still visible on the charred frame of the icon.