The church, built in 1907 by the well-known Astrakhan philanthropist and merchant Ivan Ivanovich Gubin, served as the family burial place for the Gubin merchants. In the same year, his brother Alexander Ivanovich Gubin was buried here. An interesting legend is associated with the church: in his youth, Alexander Ivanovich was attacked by Cossacks, who beat him with whips, causing his head to tremble. In the early 20th century, when the holy righteous Father John of Kronstadt visited Astrakhan, Alexander Ivanovich sought spiritual support from him. Father John blessed him with the words: "A temple will be on your body." This prophecy came true, and soon after the death of his brother, Ivan Ivanovich Gubin was buried in a specially arranged crypt under the vaults of the new church.

The church was named in honor of the heavenly patron of Ivan Ivanovich, who was born on the day of the Beheading of St. John the Baptist. On August 29, 1907, it was consecrated by the rector of the Astrakhan theological seminary, Archimandrite John Levitsky. The church was made of stone, had a single altar, was small, and lacked a bell tower. Services were held only in the summer and exclusively at the request of the Gubin family, as the church was not heated.

After the 1917 revolution, the John the Baptist church was rarely used and almost always remained closed. In December 1943, the Astrakhan Archbishop Philip Stavytsky actively sought the return of the church to the diocese and its reopening for services. In 1949, in connection with the visit of His Holiness Patriarch Alexius I of Moscow to Astrakhan, the local authorities registered the cemetery church community.

Today, the old cemetery is no longer used for burials, but the cemetery church still receives the deceased for funeral services, following an old tradition.