In 1755, the Grad-Orenburg Entry Cathedral was laid at the state's expense. Its construction was completed, and on July 12, 1758, the cathedral was consecrated by His Grace Gabriel, Bishop of Kazan. The cathedral has three altars: the main altar is dedicated to the Entry of the Most Holy Theotokos, the right chapel to the righteous Prince Alexander Nevsky, and the left to Alexius, the man of God. Until 1895, this church was called the winter Cathedral to distinguish it from the summer Transfiguration Cathedral located on the banks of the Ural River.

In 1859, with the opening of the Archdiocese in Orenburg, the church became the Cathedral Church. However, on July 18, 1931, it was completely destroyed. On April 5, 1996, the parish of the restored first Cathedral of the Entry was registered in Orenburg.

On the parish grounds, a chapel was built in honor of the Tabyn Icon of the Mother of God, the altar of which was consecrated in 2003. On April 27 of the same year, the first service was held in the revived church of the Tabyn Icon of the Mother of God. In 2007, the restoration of the first Cathedral of the Entry in Orenburg began, with the foundation poured on the preserved base. In 2010, the construction of the Entry Church intensified, and on May 24 of that year, a prayer service was held to commence the work.