The church is located near the cemetery of Bernkastel. It was probably built at the beginning of the 15th century outside the gates of the city the Gate of the Holy Spirit (which was demolished in 1872 because of the new road) for the poor and single. The Heilig Geist Armenstiftung, probably the oldest charitable foundation in the city, still exists today.
The altar of the Holy Spirit is first mentioned in documents in 1542. The current church building was erected in 1673, after the previous building was demolished due to dilapidation. In 1927, the street front was renewed in Gothic style, as was the ridge turret. The last major renovation was completed in 1982.