In the autumn of 1900, the residents of Orenburg were preparing to celebrate the 150th anniversary of the consecration of the Transfiguration Church, known as the "Golden" cathedral due to the gilded lanterns on its dome and bell tower. In 1899, the Orenburg Scientific Archive Commission proposed to restore the cathedral status to the Transfiguration Church. The main reason was its historical significance as the first stone church in the Orenburg diocese, which had remained the main church in the city for almost 150 years. In the second half of the 18th century, it was considered the main church of the entire Orenburg region and was cathedral until the new Kazan Cathedral was built. This proposal was also an expression of gratitude to I.I. Nepluev, who contributed to the construction of Orthodox churches in the region. However, the diocesan authorities did not support this initiative.

The construction of the church began in the spring of 1746 and was completed with the consecration on November 12, 1750. The church was built at the initiative of I.I. Nepluev, the founder of Orenburg at its current location and the first governor of the region. On the wall of the church, there is an inscription confirming this: "It was completed and consecrated by the blessing of the Most Reverend Luka, Bishop of Kazan and Sviyazhsk, through the efforts of the Most Exalted Lord, Actual Privy Councillor and Knight Ivan Ivanovich Nepluev. On the 12th day of November, in memory of our holy father John the Merciful." This day was likely chosen in honor of Nepluev's angel day, who was born on November 5. For the consecration of the church, Nepluev invited Bishop Luka of Kazan, who could not come and sent instead the protodeacon of the Annunciation Cathedral from Kazan. In honor of the holiday and the day of arrival of the first settler convoy on November 21, 1735, Nepluev named the first Orenburg church "Transfiguration" and the second "Introduction."

Until the early 1930s, the historical churches of Orenburg adorned the cityscape on the banks of the Yaik-Ural. In March 1931, local authorities decided to demolish the Transfiguration Church, and it was dismantled for bricks. Today, on the site of the first solidly built church in Orenburg, there is a transformer substation located near the city museum.