In 1571, Kasimov is mentioned in the land books of Peter Voieikov as a wooden city with the Ascension of Christ cathedral and an altar in honor of the Beheading of John the Baptist. However, on June 3, 1679, this church burned down, as confirmed by a petition from the cathedral priest to Metropolitan Joseph of Ryazan. The surviving cathedral icons were transferred to the Pushkarskaya Nikolayevskaya church. Although the exact dates of the new church's construction are unknown, historians attribute it to the 17th century. At the beginning of the same century, this church also burned down. The stone five-domed Ascension Cathedral with an altar of John the Baptist was laid with the blessing of the Most Reverend Alexius Titov. Construction began on March 27, 1748, funded by Voivode Vasily Mikhailovich Khovrin, and was completed with the consecration on June 13, 1754, by Metropolitan Dmitry Sechenov.

In 1779, a stone bell tower was built in place of the wooden one, financed by Vasily Andreyevich Gubarev. In 1876-1878, the church was renovated: the altar was expanded, a new iconostasis was installed, and the walls were painted. On August 8, 1787, the church was consecrated by Archimandrite Ioannikiy of the Solotchinsk Monastery along with Cathedral Protopriest Fyodor Ipatiev. By 1790, thanks to the efforts of V.A. Gubarev, two altars were arranged in the church: on the right, in the name of the Beheading of John the Baptist and Saint Basil the Great, and on the left, in honor of Saint Dmitry of Rostov and Saint Catherine. The church was consecrated in 1790 with antimins from the Assumption Cathedral. In 1837, it was visited by the heir to the throne, Alexander Nikolaevich. In the 19th century, a new cathedral with altars of the Protection and the Precursor was built, construction of which began on June 25, 1854, and was completed in 1867. The design of the cathedral was taken from the cathedral in Gatchina, as reported in the Ryazan diocesan reports of 1897.

In the 1920s, the cathedral was closed and was under the control of the Renovationists for some time. In 1936, at the initiative of the Ryazan Aero Club, a parachute tower was set up on the former bell tower. In 1960, the bell tower was dismantled. The Ascension Cathedral was returned to the Church in 1998, and in 2001, its restoration began with the support of benefactors.

The solemn consecration of the cathedral took place on July 1, 2002, under the leadership of His Holiness Patriarch Alexius II of Moscow and All Russia, with the co-serving of five hierarchs: Simon of Ryazan and Kasimov, Eugene of Nizhny Novgorod and Tambov, Joseph of Shatsk, Alexander of Dmitrov, and Theognost of Sergiev Posad. Among the clergy was Archimandrite, now Nizhny Novgorod Archbishop George.

The side altars of the cathedral: the right, of the Protection, and the left, of the Beheading of Saint John the Baptist. Currently, only the right altar is consecrated. Since 2006, on the feast of the Ascension of Christ, processions have been held at the Resurrection Cathedral.