The original, probably still wooden church, was built in the first half of XIII century, shortly after the conquest and Christianization of Dorpat by the Order of Livonian Brothers of the Sword. The oldest fragments of the present church come from the fourteenth century. In 1323 it was mentioned for the first time in written documents. In the second half of the 14th century, a tower was built by the west facade.
Revolt of iconoclasts during the Reformation in 1524-1526, the church survived without major losses. Damage was brought by the Livonian War between the Polish-Lithuanian state and Sweden, Denmark and the Rus Empire. After the end of the conflict, the church was rebuilt, but again suffered heavily during the Great Northern War. In 1704 Tartu, which at that time belonged to Sweden, was occupied by Russian troops, systematically destroying the city. The upper part of the church tower, the central nave and the chancel were destroyed. An altar and a precious pulpit burned down as well. It was not until 1737 that the restaurant of the church began, on the occasion of which the baroque Munich Chapel was added from the south. In the years 1820-1830, the interior of the church was thoroughly rebuilt in the classicism style. In 1944, the church was destroyed due to a fire caused by violent battles between the Red Army and the Wehrmacht. The church remained in ruin for a long time, which in 1952 led to the collapse of the northern wall of the nave. Reconstruction began only in 1989, and was completed in 2005.
Church of St. John is a three-nave building in the form of a basilica, to which the tower adjoins from the west, and from the east an elongated, polygonal ended chancel. On the north side of the chancel there is a sacristy. At the southern part of the nave there is medieval, so-called Lübeck Chapel. The tower was built on a square plan, it is an extension of the nave and rises to a height of 63 meters. The outer walls of the church are decorated with friezes and blendes. The western portal was crowned with a stepped wimperg with fifteen figures in niches.
The pride of the church are the unique, separately modeled figures from terracotta from the fourteenth century. Originally there were about two thousand of them. Many of them were unfortunately destroyed during the rebuilding of the church and as a result of fires and wars, but more than half of them have survived to this day. They depict figures of saints, but there are also images of fantastic animals and grotesque devils. Each figure was hand-cut in wet clay, so that each of the images differs from the others. It is possible that the pattern for these sculptures was the faces of women and men living in the city in the fourteenth century. Initially, their number exceeded the sum of all other terracotta sculptures created in the Middle Ages in Western Europe. The originals are currently in the nearby museum, while in the church are their accurates copies.