The the Holy Spirit Church, the current parish church, was begun in the late 15th century. It was built by a Catholic begging order, which only came to Denmark quite late in the Middle Ages, where they built a total of five monasteries. Before the Holy Spirit brothers settled in Faaborg, the city had a Holy Spirit house where old, sick and poor could get help.

In 1477 the monastery was founded in Faaborg, and on March 14th of 1478 it was approved by the pope in Rome. The church appears today as a large and beautiful church with monastic chairs from Catholic times. The old baptismal font of granite is from the Middle Ages, and a Catholic cupboard from the late Middle Ages has been transferred from the first Sct. Nicolai Church.

The original altarpiece of the Holy Spirit Church from 1511 is now found at the National Museum in Copenhagen and is a treasure from this time. The current altarpiece is from 1855 and painted by Vilhelm Marstrand. The organ has 34 voices and is from 1979. The church is yellowwashed and has no tower, but a chipboard equestrian spire.