The town church in Creuzburg is one of the first Protestant churches in the whole of Thuringia. Today it is a listed building. It took three years to build, from 1215-1218, and was probably originally planned as a Romanesque basilica. The large, semi-circular choir room with a diameter of 11 meters bears witness to this. Due to its size, the church could not be fully completed in the 13th century. Miraculously, it was one of the few buildings to survive a siege by King Adolf von Nassau in the summer of 1295. The church was finally completed in the 14th century, but it still did not have a tower. This was not erected until 1428. Although the rich furnishings of the Nikolaikirche were severely vandalized by religious zealots and iconoclasts during the Reformation, the building itself survived the Peasants' War and the Thirty Years' War that soon followed unscathed.

However, St. Nikolai burned down completely in a major fire in 1765. At that time, even the privy councillor Johann Wolfgang von Goethe traveled there, sketched the ruins and became involved in the reconstruction. However, it took almost 20 years before reconstruction could begin. The church was re-consecrated in 1786. The interior decoration was adapted to the taste of the time and an organ was purchased. In 1921, a memorial plaque was erected to the Creuzburg composer and organist Michael Praetorius, who was an important representative of Protestant church music. He was born in Creuzburg in 1521. He penned works such as „Es ist ein Ros‘ entsprungen“ and „In dulci jubilo“.

However, the effects of the Second World War did not leave the church unscathed. A heavy attack by American troops completely destroyed the church. It was burnt to the ground and remained in this desolate state as a ruin and memorial until the 1960s. Reconstruction began in 1963 and maintenance and renovation work continues to this day.