St. John's Church was first mentioned in written sources in 1297. After several reconstructions, around 1500 the church acquired its present appearance – a high Gothic stepped gable, a span roof and a small tower.
Until 1523, St. John's Church belonged to the Dominican Order. The Latvian congregation acquired it in 1582. However, it turned out to be too small for the Latvian Lutheran congregation in Riga, as a result in 1587–1588 the church was enlarged with a new altar extension.
The present church tower was built in 1849 according to a project by architect Johann Daniel Felsko.
There is a legend connected with St. John's Church. In the 15th century, two Dominican order monks wished to become canonised, so they were immured alive in the church wall. While the two monks were still alive, Riga residents fed them through a special hole left in the wall. However, at the end they were not consecrated. To commemorate the monks a cross-shaped hole was made in the outer wall of the church.