The construction of the stone church in honor of the Smolensk Icon of the Mother of God began in the 1680s by the order of Grigory Dmitrievich Stroganov. A similar church was also founded in Ustyuzhna-Zhelezopol.

The chapel dedicated to the Kiev-Pechersk miracle workers Anthony and Theodosius was consecrated by the Nizhny Novgorod Metropolitan Pavel on December 22, 1694, and the main altar in honor of the Smolensk Icon of the Holy Mother of God was consecrated on July 25, 1697.

After the Stroganov family moved to Moscow in 1705, the Smolensk church became a parish church. It was closed in 1930, and in 1934 there were plans to blow it up. However, thanks to the efforts of the staff of the Gorky Regional Museum, the building was preserved. Until the early 1990s, it was used as a museum storage.

In 1993, the church was transferred to the diocese. In 2005 and 2006, the main dome was gilded.

In 2018, repair work began, and in 2019, a large-scale restoration started aimed at restoring the historical appearance using 3D models and white stone carvings. The completion of the work is planned for the 800th anniversary of Nizhny Novgorod in 2021.