The wooden Church of the Nativity of John the Baptist in Nizhny Posad has been known since the 15th century. In the early 17th century, it included a refectory and a porch.

In 1676, merchant Gavriil Dranishnikov, returning from Astrakhan, received the blessing of Metropolitan Filaret to build a stone church at his own expense. This was to confirm his commitment to Orthodoxy, as his wife Anna and son, having become Old Believers, fled to the Kerzhensky sketes. After Dranishnikov's death on August 24, 1679, his brother Lavrentiy completed the church, adding a southern chapel in honor of martyr Anna in memory of his wife.

The church, designed in the shape of a ship, stood on a high brick sub-church with benches rented out to merchants. In 1814, a Dukhivskoy chapel was added to the northern side of the refectory.

As a result of urban planning changes in 1834 and 1839, it was ordered to remove buildings around the Kremlin, which led to the destruction of the drainage system and undermining of the foundations. Repairs in the 1830s-1840s were carried out by architects Anton Leer, Ivan Yefimov, and Georg Kizevetter.

In 1855, a tent chapel of Alexander Nevsky and a watchman's lodge were added to the church. In 1870, the bell tower was reconstructed. Repair work was again needed in 1881 and 1885, and in 1899, after a break in the iron connection, the altar was relaid.

In 1937, the church was closed, and the last rector was shot. During the Soviet era, the building housed a motorcycle sports school of DOSAAF.

In the 1990s, the church was returned to the Nizhny Novgorod diocese, and services resumed in 1994. In June 2004, restoration work began, funded by patrons, of which 60 million rubles were provided by the Balakhna Pulp and Paper Mill. On April 4, 2005, three new crosses for the domes were consecrated, two of which were already installed. On August 5, 2005, a dome and cross were placed on the bell tower. On November 4, 2005, the church was consecrated by Patriarch Alexy II of Moscow and All Russia. During the repairs, services continued without interruption.

During the restoration, a supporting concrete wall was built, and zero marks were returned to the level of the 19th century.

In 2009, an Orthodox lecture hall began operating at the church.