The church was founded at the end of the thirteenth century, then still as a two-nave 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 and a tower sunk into the temple on the west side. It was built in 1433. Shorter walls of the building are decorated with gothic crow-stepped gables. The chancel is unusually arranged, because it is asymmetrically placed in relation to the two-nave corpus. Around 1360 a wooden, flat ceiling was replaced with vaults and new, larger, gothic windows were pierced. Inside, medieval gothic equipment is distinguished by a gothic cross and a valuable altar of master Bernt Notke from 1483.