The history of the church begins in 1700, when residents Grigory Koshkin, Zakhar Eliseev, and Yakov Anikeev moved from the parish of the Assumption Church, where shipbuilding had begun, to the Akatovskoye suburb. In October of that year, they appealed to Emperor Peter I, who was in Voronezh, requesting permission to cut down trees for the construction of a new church, which they wanted to dedicate to the Assumption of the Mother of God. The church was soon built and consecrated by Saint Mitrophan, the first bishop of Voronezh. It is likely that the Saint considered it inconvenient to have churches with the same name in the city, and the new church was named the Vvedensky.

In 1780, the wooden church was replaced with a stone one, featuring two altars. In addition to the main altar, a chapel was established in honor of the martyr John the Warrior, and in the 19th century, another chapel was added, dedicated to Saints Mitrophan of Voronezh and Tikhon of Zadonsk. The church has long been considered one of the most beautiful in the city, its architecture bearing the features of the famous architect of the 18th century, B. Rastrelli.

By the beginning of the 20th century, the parish of the Vvedensky Church numbered 77 households. Since 1887, a charity for underprivileged parishioners operated at the church, and from 1891, the first parish school with "handicraft classes" in the diocese was established. The famous Russian writer Ivan Bunin was baptized in this church.

In a small cemetery by the church rest the priests who served here and pious laypeople, mostly from the merchant class. The names of some of them have been preserved in the chronicle "Synodic," but the graves themselves were destroyed in the infamous years.

In the mid-1930s, the Vvedensky Church was closed. For several decades, its building was used by various organizations and gradually fell into disrepair.

In 1999, the Vvedensky Church was returned to the diocese. "We acquired this church as a gift from God," noted the ruling bishop of the Voronezh-Lipetsk diocese, Bishop Mephodiy (Nemtsev). On December 4, 1999, on the feast day of the church, the restored church was consecrated by the ruling bishop, and the Divine Liturgy was celebrated there for the first time after many years of desolation. Since then, early Liturgies have been held here every Sunday and on major feast days, and throughout the week, sacraments are performed: baptisms, weddings, and funerals. The church is adorned by the work of the sisters of the monastery and local icon painters. The icons of the multi-tiered iconostasis, carved beams, and icon cases are made according to ancient patterns.

In February 2002, bells cast from donations by parishioners were raised to the bell tower. The names of the benefactors are inscribed on the largest of them. Now, just like a century ago, the sound of the bells resonates over Vvedenskaya Street with its old houses and gardens, calling people to the house of God for prayer.