The church was built in 1731 with funds from landowner Pyotr Mikhailovich Argamakov. In 1936, the Soviet authorities closed the Glukhovo church, and the priests were arrested and exiled. The building was used by the Stalingrad collective farm as a grain storage facility, and on June 8, 1940, the district executive committee transferred it for use as an MTS workshop and power station. Later, to facilitate its use, the supporting pillars of the church were dismantled and the entrances were widened. On a Sunday in June 1947, the church collapsed and was dismantled to the ground. The bell tower survived, but in 1984, its wooden dome burned down due to a lightning strike.

In 2001, Nizhny Novgorod resident Alexey Silaev, who bought a house in Glukhovo, restored the bell tower's dome. In 2003, the recently appointed Bishop Georgy visited the village. In 2004, several women, led by Valentina Golyakova, registered a church community, planning to build a small wooden church. The residents sought help from the ruling archbishop. One of the benefactors was Ilya Gubin, president of Novikombank, who was awarded the Order of the Venerable Seraphim of Sarov III degree. The project was developed by church architect Andrey Anisimov, and the restoration and construction were carried out by his workshops. The construction work was led by priest Igor Borisov. On July 21, 2009, Archbishop Georgy laid a commemorative capsule with a certificate at the foundation of the building church. The ceremony was attended by Archbishop Sergey of Ternopil and Kremenets, who noted that the revival of earthly temples contributes to the revival of the temple of the soul.

Ten bells for the church were made at Nikolai Shuvalov's factory in Tutayev using the "clay casting" technology, which ensures special strength and pure sound. The cross and bells were consecrated by Archbishop Georgy in October 2009.

Since February 2010, the parish has been led by priest Igor Borisov. On September 14, 2010, Archbishop Georgy consecrated the chapel in honor of the Prophet Elijah and served the first Divine Liturgy. Archpriest Igor Borisov noted that in the 1920s, a revolutionary council met in Glukhovo, which closed the Diveevo Monastery, and after eight decades, justice has triumphed.

On November 6, 2010, Archbishop Georgy performed the rite of consecration of the main altar of the church, assisted by Archpriest Igor Borisov. At the consecration, the parish was gifted an ancient icon of the Mother of God "The Sign" and a large mosaic icon of the Savior from Andrey Anisimov's workshops, which now adorns the main entrance to the church.

In December 2010, work was completed on the four-tier iconostasis in the main chapel. Specialists from the "Ark" workshop used icons from the Russian iconographic school of the 15th-16th centuries. The body of the iconostasis was made according to the traditions of the ancient Kostroma school of carving, characteristic of the churches of the Moscow Kremlin, with toning and colored enamel.

On February 23, 2012, Archbishop Georgy performed the great consecration of the chapel in the name of Venerable Alexius, the man of God.