In the 17th century, there stood a church known as Nicholas on the Square at the site of the current temple, which was transferred to the Assumption Monastery in 1723. By the early 19th century, the building had deteriorated significantly, and in 1842, a new two-story five-domed church in honor of the Transfiguration of the Lord was erected on its site according to the design of V. F. Fedoseev. This church is a vivid example of Russian classicism from the early 19th century, with its facades adorned with Doric columns.

The main altar of the lower church, dedicated to the icon of the Most Holy Theotokos "Relieve My Sorrows," was consecrated in 1836. The first floor also housed two altars: in the name of Archangel Michael and Saint Barbara the Great Martyr. The main altar of the new church, dedicated to the Transfiguration of the Lord, was located on the second floor and was consecrated in 1842. The southern chapel of the upper church was dedicated to the Tikhvin Icon of the Most Holy Theotokos, while the northern chapel was dedicated to Saint Nicholas the Wonderworker, in memory of the previous church. The chapels were consecrated in 1843.

The northern and southern facades of the church are adorned with colonnades of eight Doric columns. Between the columns are large windows, which allowed ample light into the upper church. The basement floor, where the lower church was located, had semicircular windows framed with wedge-shaped stones. At the entrance to the church was a tent-like tambour, a later addition in the Russian style, which did not quite harmonize with the classicist appearance of the Transfiguration Church.

On the eastern side of the church, along the northern wall of the monastery fence, there was a bell tower with seven bells above the main gates. It faced Lopatinskaya Street, now Mendeleevskaya, and was situated between the Transfiguration Church and the abbess's cells. On the second tier of the bell tower was a small church of the Sign of the Most Holy Theotokos, which had a passage leading from the abbess's cells. The bell tower, the Transfiguration Church, the stone fence, and the towers at its corners formed a harmonious architectural ensemble.

The main shrine of the Assumption Monastery, kept in the Transfiguration Church, was the icon of Saint Nicholas the Wonderworker, known as the "Tula" icon. According to legend, in the 16th century, one of the Dnieper Cossacks found the icon of Saint Nicholas the Wonderworker in a swamp in Tula, built a church in his honor called "Nicholas on the Square," and placed the found icon there. This icon was especially venerated by Cossacks and warriors, believed to have helped the city's defenders repel the attack of the Crimean Khan Devlet Geray in 1552. After the October Revolution, the icon was lost.

During the Soviet era, the church building was significantly altered, losing four of its five domes and resembling a secular structure. This impression was heightened by the absence of an altar apse in the eastern part. The bell tower was destroyed in the early 1920s, and the Transfiguration Church was handed over to a weapons factory. The basement was used as a warehouse, while the upper floor was occupied by Proletkult institutions. Later, the building housed a communal service department, and from 1949, the Tula Committee of DOSFLOT and a Naval School. In 1960, the Transfiguration Church was placed under state protection as a monument of 19th-century architecture.

At the end of 1993, the church was transferred to the Tula Orthodox Classical Gymnasium. From 2001 to 2007, restoration work was carried out: two floors were arranged, and four lost domes were restored. A Sunday school and a video library with Orthodox themes operate at the church.