The wooden church in honor of the Vladimir Icon of the Mother of God likely existed since the early 17th century until it was destroyed by fire. It was located in the lower part of the city, behind the fortress walls, and its parishioners were wealthy owners of Arzamas leather factories. In 1681, Patriarch Joakim issued a decree for the construction of a stone church on the same site, with the condition that the domes would not be tent-like and the altar apse would be triple. More than a hundred years later, the church was dismantled and a new, cold one was built, consecrated on March 23, 1802, by Archimandrite Ioann of the Makaryev-Zheltovodsky Monastery. Later, two chapels appeared in the adjoining refectory: the right one in honor of the Venerable Zosima and Savvatiy of Solovki, and the left one in honor of St. Dimitry of Rostov.

Before the closure of parish churches during the period of persecution, the church was referred to as Zosimovsky or Izosimovsky, which indicates the veneration of the Solovki saints. This is related to the fact that some parishioners were descendants of those resettled to Arzamas from Veliky Novgorod.

In 1866, the third male parish school in Arzamas opened at the Vladimir Church.

During the godless five-year plan, the parish was closed, and the churches were liquidated. The iconostasis of the Vladimir Church was sold abroad, and the building was repurposed as a masonry workshop, later a bakery. The Epiphany Church was temporarily used as a dormitory for prisoners in 1931 but was destroyed within five years.

The heavily reconstructed and dilapidated building of the Vladimir Church began restoration in the winter of 2003-2004. By spring, it was possible to clear the premises of debris and partitions, dismantle the roof, cutting down the trees that had grown on it, and board up the windows.