It was first mentioned without a doubt in a document in 1287 and at that time still belonged to the municipality of St. Martin as a "branch". At that time, however, it was still a predecessor building, which is more likely to represent a chapel than today's church. The municipality of St. Johannis received its independence on May 9, 1349 at the instigation of the knight Rapoto von Külsheim. He is also considered the founder of the parish.
In 1380 the church received an enclosing wall, which, however, could not protect the church from being severely damaged and burned down in 1449 during the First Margrave War. As a result, the church building was rebuilt and almost in its present form. A foundation in 1499 is likely to have led to the expansion of the tower with its four spiers and impressive roof. Remains of the previous building are preserved in the two lower tower floors. The church bells consist of a total of four bells that were brought in between 1450 and 1954. In 1518 the southern portal porch and the Mount of Olives scene were completed.
After severe devastation in the Thirty Years' War, the church was rebuilt piece by piece from 1688 to 1738 and partially redesigned. It largely got its current appearance. During these fifty years, the interior was also heavily redesigned in the Baroque style. The altar, the pulpit, the two galleries and the organ date from this period.
There is a cemetery on the west front of the nave, but it has not been used since the early 19th century. At this time, the new Burgfarrnbacher Friedhof on Oberfarrnbacher Straße was inaugurated.
In the former defensive towers at the corners of the tower, kestrels have been breeding for years. In 2008, a pair of peregrine falcons established themselves to nest. They raised four young birds.