The Church of St. John the Theologian is considered an important historical shrine of the capital of Mordovia. It is one of the oldest landmarks of Saransk and the entire republic, a rare gem of the region. The history of the temple of the great evangelist likely began in the early 17th century. The modern building dates back to 1700, although some sources indicate 1693. The church is located in the center of Saransk, which was originally a fortress on the border, protecting against raids by the Nogai Horde and Crimean Tatars.

Historical records indicate that the baptism of the Mordvins began in the 16th century and was completed by the middle of the following century thanks to local Orthodox churches. Saransk was built near already existing settlements, such as Ivanovskoye, where the first church in honor of St. John the Theologian was built in 1600. This wooden church remained active for more than a hundred years after the construction of a new stone temple, which was also consecrated in the name of St. John the Theologian. In 1824, it was dismantled and moved to the village of Makolovo.

The exact dates of construction for many Russian churches are often lost, but the time of the erection of the Church of St. John the Theologian can be determined with certainty. In 1873, during the removal of the covering from the altar, an antimins dated 1600 was discovered. When it was time to build the stone structure, craftsmen were invited from Moscow or Nizhny Novgorod. The new church was built in the Moscow Baroque style, known as Naryshkin Baroque, which was popular in Russia from the late 17th century.

In 1711, a bell tower and refectory were added to the church, and later two chapels appeared. The church survived the fires of 1817, 1852, and 1869, which destroyed much of wooden Saransk. Before the 1917 revolution, the church had arable land and forest lands. The staff consisted of two priests, one deacon, and two psalmists.

After the October Revolution, mass looting of churches began. The Church of St. John the Theologian in Saransk miraculously survived. In the 1930s, it was closed, citing a decrease in attendance. However, the building stood empty, and soon the church was returned to the faithful. In 1938, it was closed again, citing dilapidation, and housed the NKVD archive, which possibly saved it from destruction.

In 1944, during World War II, the church became active again. In 1946, it was renovated, the frescoes were restored, and the walls were plastered. In 1960, the church received the status of a federal architectural monument.

In the post-war years, the church was restored by the community. In the 1970s and 1980s, it regained popularity. In 1991, the Saransk and Mordovian Diocese was established, and the church became the cathedral until the construction of a new cathedral in honor of Feodor Ushakov.

In 2002, a spiritual and educational center was built on the parish grounds with a baptismal church, consecrated in 2003. The main altar of the church is dedicated to St. John the Theologian, the right one to the Annunciation of the Most Holy Theotokos, and the left one to St. Nicholas the Wonderworker. The church houses a revered copy of the Vladimir Icon of the Mother of God from the 16th century.