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The Church of John the Baptist in Kerch was built in the 10th century by Byzantine builders, with the foundation and part of the walls preserved from the 6th century Christian church. In Kiev and Novgorod, as well as other cities of Kievan Rus, churches of the 11th century have been preserved to this day. Thus, the Church of John the Baptist in Kerch can be called the oldest Christian church in Russia. 

Archaeologists and historians argue about the exact dates of the construction of the church, but in any case they are older than St. Sophia Cathedral in Kiev (1037) and St. Sophia Cathedral in Novgorod (1045). The first temple on the site of the Church of John the Baptist was built in the 6th century, during the reign of Emperor Justinian. The Byzantine Empire was then in its heyday. At the same time, the Hagia Sophia in Constantinople was built.  

The foundation, fragments of the external altar walls and columns have been preserved from this ancient church. They can now be seen in the Church of John the Baptist. In the 10th century, the church was partially destroyed during the storming of the city by the squad of Prince Mstislav Vladimirovich, but it immediately began to be restored. 

During the reconstruction of the 10th century, Byzantine builders recreated exactly the architecture and interior of the ancient church of the 6th century. They also preserved the special brick masonry from the plinth, which was used by the masters of the 6th century. In the 14th century, almost the entire Black Sea coast from Kerch to Balaklava came under the rule of the Genoese. They restored the Church of John the Baptist, but also preserved the original appearance of the ancient Byzantine temple.

During the Turkish rule, the Church of John the Baptist became a mosque, which saved it from destruction. After Crimea became part of the Russian Empire in 1783, the church became Orthodox again. In 1834 a new chapel was added to it, and in 1845 a bell tower was built. At this time, the church of John the Baptist acquired the appearance that we see now.