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The Church of the Icon of Our Lady of Iveron is the oldest church in Feodosia. It was built in 1348 near the wall of the Genoese fortress of Kafa in the Armenian quarter of the city. In total, there were five churches in this quarter, four of which have survived to this day. The ruins of the fifth temple were found during excavations. 

The population of Kafa during the time of Genoese rule consisted of 2/3 ethnic Armenians. After the construction of the outer walls of the Genoese fortress of Kafa, some Armenians founded their own commune and settled near the eastern wall. Later they enclosed their commune with a wall and called this quarter Ayots Berd (Armenian Fortress). Here they built five churches, the Church of the Icon of Our Lady of Iveron is the largest of them.  

After the construction was completed, the Armenian church was consecrated in honor of John the Baptist. In 1474, the famous Russian voyager Afanasy Nikitin spent several winter months in the Kafa. He returned from a trip to India and rested in the city.  
Here he also worked on his book "Walking across Three Seas". In the church of John the Baptist, he prayed to return healthy to his native Tver. He left city just a few months before the Turks invaded Crimea. In 1475, the Turks stormed all the Genoese fortresses in the Crimea: Kafa, Sudak and Balaklava.  

Afanasy Nikitin left Kafa with the last Russian trade caravan, but did not reach his native Tver. He died of an illness in Smolensk. In memory of Afanasy Nikitin`s stay in the Kafa and his prayers in the church of John the Baptist, his monument is installed next to the temple. 

During the reign of Catherine II, Armenians were relocated from Feodosia to the Low Don River, so the Ayots Berd area fell into desolation. Given that the area was fenced off by a wall, it began to be used as a place for quarantine. All those who returned from Asian countries were obliged to spend 40 days in the Ayots Berd quarter. 

In 1875, the Armenian Church of St. John the Baptist became an Orthodox church, which was consecrated in honor of the Icon of Our Lady Iveron. Now both names of the temple are used: the Church of the Icon of Our Lady Iveron and the Church of John the Baptist. Because of this, there are sometimes inaccuracies in the names, especially since the Church of St. John the Theologian is located nearby. John the Baptist and John the Theologian are different people.   

According to ancient chronicles, the frescoes in the Church of the Icon of Our Lady Iveron were painted in the 15th century by the famous Russian painter Feofan the Greek. In Soviet times, the church was closed and used as a warehouse, so the ancient frescoes have not been preserved. There is only one church in Russia where the frescoes of Theophanes the Greek have been preserved: the Church of the Transfiguration of the Savior on Ilyin in Veliky Novgorod.