The church is located on the grounds of the Holy Trinity Seraphimo-Diveevo Convent in Nizhny Novgorod, which was opened in 1997.

The area of the Exaltation of the Holy Cross Square, now known as Lyadov Square and Polevaya Street, modern-day Gorky Street, began to be actively developed in the mid-19th century. Residents of the new part of the city persistently requested the spiritual authorities to build a church in this area, as the nearest Pokrovskaya Church was difficult to access due to deep ravines and turbulent streams in the spring and autumn.

Bishop Jeremiah supported the parishioners' desire and appealed to the military governor F. V. Annenkov to designate a location for the construction of a new church. The intersection of Kanatnaya and German Streets was chosen. The bishop also determined the dedication of the future church: "so that the locality and the church would be dedicated to the name of the celebrated here First-Called Russian Saints, guardians of apostolic traditions, mentors of Orthodoxy, and protectors of our Fatherland Peter, Alexius, and Jonah."

The architect of the church was N. I. Uzhumetsky-Gritsevich, and in April 1859, the laying of the foundations began. By the following year, the stone church was fully constructed. Inside, the floor was laid with white stone, three carved iconostases were installed, the vaults were decorated with frescoes, and the walls were covered with canvases depicting saints. Seven bells on the church's belfry delighted the residents of Nizhny Novgorod with their ringing.

By the end of 1860, it was reported to the Synod that the stone Trinity Church in Nizhny Novgorod was built "in all parts solidly, elegantly, and cleanly."

On December 1, 1860, Bishop Nectarios of Nizhny Novgorod consecrated the main altar of the church in honor of Peter, Alexius, and Jonah, Moscow miracle workers. On December 14, the right chapel was consecrated in honor of the Apostle Jason and St. Nicholas the Wonderworker, and on December 16, the left chapel was consecrated in honor of the Evangelist Luke.

In the 20th century, the Trinity Church shared the fate of many churches in Russia. After the 1917 revolution, the church was desecrated, and a dormitory was arranged in the prayer hall. In 1998, restoration of the church began with funds from the Holy Trinity Seraphimo-Diveevo Convent.

On June 11, 2004, Bishop Georgy of Nizhny Novgorod and Arzamas consecrated the main altar in the name of the saints Peter, Alexius, Jonah, Philip, and Hermogenes, Moscow and all Russia miracle workers, whose feast day is celebrated on October 18.