In the early 17th century, a wooden "Church of Tsar Constantine" stood on the site of the current church. The parish was small, and the clergy received salaries from the state treasury thanks to gun grants, which is why the church was referred to as "gun" in the Suzdal inventory.

The old wooden church was dismantled due to its dilapidation, and in 1707, a stone church was built with funds from the parishioners. This was the last five-domed church erected in Suzdal. The temple was used in the summer, while a low winter church in honor of the Icon of the Sorrowful Mother of God was located nearby. It is likely that in the late 18th century, an altar apse was added to the church. In the first half of the 19th century, a round narthex with three porticos in the Empire style appeared on the western side, which harmoniously blended into the architecture of the temple despite the differing styles.

In 1923, the temple was closed and turned into a linen warehouse, and later a garage. In 1976, before the church was handed over, the building housed a public toilet. The church was then transferred to the Russian Orthodox Church instead of the closed Kazan church in the central square of the city. Valentin Rusantsov became the rector, under whose guidance the church was completely restored in six months.

In 1988, the relics of Saint Euphrosinia of Suzdal and Euthymius of Suzdal were transferred from the Suzdal museum to the church. On April 7, 1990, Archimandrite Valentin Rusantsov and members of the community announced their exit from the Moscow Patriarchate, and on April 11, they were accepted into the jurisdiction of the Russian Orthodox Church Outside Russia. On October 4, Archimandrite Valentin became the Exarch of the Archdiocesan Synod of the ROCOR in the territory of the USSR.

In June 1995, after the final separation of Valentin Rusantsov from the ROCOR, the Church of Tsar Constantine became the cathedral of the unrecognized "Russian Orthodox Free Church" he established, later renamed the "Russian Orthodox Autonomous Church" (ROAC).

On February 5, 2009, the Arbitration Court of the Vladimir Region ruled to seize the church from the ROAC along with nine others. On August 19, 2009, the last liturgy was held in the cathedral, and on August 20, the church was handed over to federal authorities.

On December 31, 2009, the Church of Tsar Constantine was transferred for indefinite gratuitous use to the Vladimir Diocese of the Russian Orthodox Church, and restoration work began in the church. On January 7, 2011, the first liturgy in many years was held under the jurisdiction of the Russian Orthodox Church.

The church is a tall pillarless square structure, covered with a four-sloped roof. An altar apse adjoins the building on the eastern side, while a narthex in the classical style is on the western side. On the white walls, like an embroidered border, stand out a wide cornice made of small and deep horseshoe-shaped kokoshniks, a frieze of crenellated towns, and balusters resembling the cornices of the bell tower of the Resurrection Church, as well as elegant decorative window finishes. Above the roof rise five slender columns with reliefs, supporting intricate domes. The ornate upper part and the play of contrasts between the simple and the complex remind one of the now non-existent Trinity Cathedral of the Rizpolozhensky Monastery.