The Church of the Holy Spirit holds a special place in Estonian cultural history. It was the first congregation that started holding services in the Estonian language (1531). Johann Koell, the pastor at the time, is the author of the oldest known book in Estonian. Together with Simon Wanradt (from Niguliste - St Nicholas'  - Church) he compiled a short cathecism in Estonian and German. The book was published in 1535.

The next pastor (in service from 1563 to 1600) is just as noteworthy. Balthasar Russow is the author of  Livonian Chronicle (Nye Lyfflendische Chronica) published in 1578. The chroncile is the prime source of information on the history of Estonia and Livonia in 16th century as well as the Livonian War.

The church building dates back to the beginning of 13th century, and served as an almshouse church as well as chapel for the city magistrate. In art history, the building is often referred to as a "museum of styles". Indeed, it exhibits well-preserved architectural elements and artefacts from different periods: main altar by master Bernt Notke (1483), Renaissance pulpet (1597), Baroque steeple, 17th century Biblia Pauperis, 17th century woodcarvings on the balcony (local master Elert Thiele), chandeleers (16-17th cent), triumphal arch (15-17th cent), pews (16-19th cent). The original bell dated back to 1433, which made it the oldest surviving church bell in Estonia. Unfortunately it was partly destroyed in a fire in 2002.  In 2003 it was replaced with an exact copy that still features the inscription from the original bell - "I strike alike for maid, madam and master. Nobody can hold that against me". On the facade, a 17th century clock is still working.

The church holds services in English, every Sunday at 15.00.