The church was founded at the end of the thirteenth century, then still as a two-aisle chapel belonging to an adjoining shelter. Primarily, it was attended mainly by sick residents of the almshouse and urban poor, but later also rich merchants gathered in the Great Guild on opposite side. Thanks to this, the church has become the most egalitarian temple in the city. The construction of the proper temple was completed in 1380.
In 1524, the local Lutherans took over the building. It soon became the most important temple for them in Tallinn. Unlike other churches, from 1531, sermons were preached here in Estonian, not in German. The pastor associated with the church of the Holy Spirit, Johann Koell, is considered the author of the oldest surviving book printed in Estonian, a catechism from 1535. In the 16th century, Balthasar Russow, one of the first Livonian chroniclers, was also a parish priest here.
In the 17th century, the church tower received a new Baroque helmet, and in 1684 the oldest in the city, the public clock, preserved to this day, was mounted on the outer wall. Also in the 17th century, side galleries were placed inside the church.
The church was built on a rectangular plan, with a nave covered with a gable roof, a straight ended chancel on the eastern side and a small, polygonal tower embedded in the nave in 1433 on the west side. The shorter walls of the building were decorated with Gothic stepped gables. The chancel was located atypically, because it is asymmetrically placed in relation to the two-aisle nave. Around 1360, the wooden, flat ceiling was replaced with vaults and new, larger, Gothic windows were pierced.
Merged into the cramped buildings of the old town, the church has preserved to this day its Gothic body, slightly obliterated from the outside with a Baroque helemet of the tower, and inside with side galleries. Among the preserved medieval furnishings, the Gothic cross and the valuable altar made by master Bernt Notke from 1483 stand out.