Historical documents indicate that a city cathedral dedicated to Saint Nicholas the Wonderworker existed in Tarusa as early as the 16th century. These documents mention royal gifts and favors granted to the Nicholas Cathedral. For example, there are known decrees from Tsar Fyodor Ivanovich from 1594 for church construction, as well as from Tsar Mikhail Fyodorovich dated December 25, 1615, for construction, candles, incense, and half of the toll on the Oka River. Tsar Alexei Mikhailovich also made donations to the cathedral.

The land registry books of 1625 state that the Nicholas Church in Tarusa was wooden and located "near the landslide," and all church property was "the State's."

In 1779, a severe fire occurred in Tarusa, leaving only 23 houses, and the wooden Nicholas Cathedral burned down. The Tarusa Spiritual Administration appealed to the Krutitsy Spiritual Consistory for permission to build a new wooden church on the same site, using suitable wood from the burned church.

On May 13, 1785, it was ordered to build a stone cathedral with a bell tower in Tarusa at the expense of the treasury, excluding the iconostasis, for 5,989 rubles. Construction was to begin in 1785 and be completed in 1787. The work, initiated by the decree of Empress Catherine II, was completed in 1789. A contract with Kaluga merchant Ivan Maksimovich Altynikov, who committed to build the cathedral, has been preserved. However, by the appointed time, the construction was not finished. An architect who inspected the site on June 5, 1786, found substandard materials, and the work was temporarily halted.

The architect of the Peter and Paul Cathedral is considered to be Ivan Denisovich Yasnigin, the provincial architect of Kaluga from 1785 to 1822. He is known as a continuer of the traditions of architect P.R. Nikitin.

On March 22, 1790, the cathedral was consecrated in honor of the holy apostles Peter and Paul. Initially, it was elongated with a three-tiered stone bell tower but without side chapels. In the 1820s, thanks to parishioners and "benevolent donors," two other chapels were built. As a result, the cathedral had three altars: of the Chief Apostles Peter and Paul, of Saint Nicholas the Wonderworker (consecrated on June 25, 1823), and of the Dormition of the Most Holy Theotokos (consecrated on October 1, 1833).

In 1871, a stone fence with an ornate iron grille was installed. Inside the fence, among fruit trees and lilacs, were the graves of clergymen. The cathedral had a main bell weighing 210 poods, and there were a total of seven bells in the belfry. The parish had schools: a four-grade city school, two city parish schools, and a church-parish school.

In the 20th century, the cathedral faced the fate of many churches: in 1933, it was closed, and clergymen were arrested and repressed. The destruction of the cathedral began around 1937. According to eyewitness accounts, the bell tower was wrapped in steel cables and its foundations were chipped away. After several attempts, the bell tower collapsed. In the square where the Lenin monument now stands, books, icons, and church utensils were burned. In the fire, old printed books, ancient icons, and other relics were lost. Church books and vestments were brought from all over the district to Tarusa and burned. The necropolis around the church was lost, and the large bell was taken to the Tarus collective farm.

During the Soviet era, the cathedral was used as a pioneer house, the building was remodeled, a stage was placed where the altar had been, and the space was divided into two floors. The revival of the cathedral began with the transfer of the building to the Kaluga diocese. On July 22, 1999, the cathedral was handed over to the diocese based on the order of the Ministry of Culture and the Ministry of State Property of the Russian Federation.

The cathedral is being restored to its original appearance while preserving all architectural details. The restoration architect is Alexander Lyubeshkin. The first prayer service and procession took place on July 12, 2001, under the guidance of Archbishop Clement of Kaluga and Borovsk.

In 2003, the octagon of the main dome was restored, and a cross was installed. In 2004, crosses were placed on the domes of the chapels of Saint Nicholas the Wonderworker and the Dormition. By spring 2005, the construction of the three-tiered bell tower was completed. Father Leonid appealed to the city's residents to raise funds for the belfry. The necessary amount of 600,000 rubles was raised, of which 200,000 was for the main bell. The names of more than eight hundred people who donated for the bell are known. On July 12, on the day of Peter, the bells were raised to the third tier of the bell tower.

The main holiday of Tarusa became the cathedral's feast day, July 12, the day of the memory of the holy apostles Peter and Paul.