The church traces its origins to a small chapel on this site dating from the early 1300s, later replaced by a brick church that was demolished in the sixteenth century. Construction of the present building began in 1580 under Johan III, but work stalled for decades after his death and the church was not consecrated until 1643, reportedly in the presence of Queen Kristina. The result is a red-rendered brick hall church combining late Gothic, Renaissance and Baroque elements, with a three-aisled nave, a narrower polygonal choir and elaborately carved sandstone portals, the southern one traditionally attributed to the sculptor Markus or Hans Hebel.
A serious fire in 1723 destroyed the original tower, roofs and Dutch Renaissance-style gable ornaments, prompting a rebuilding that gave the exterior its present classicist and late Baroque character. The distinctive copper-clad central tower, completed in 1739 to a design associated with Göran Josuae Adelcrantz and Carl Hårleman, is considered an unusually accomplished example of late Baroque tower design in Sweden.
The interior has been altered repeatedly. A nineteenth-century restoration under Carl Möller reduced the choir's large windows and introduced a National Romantic decorative scheme, while a further restoration in the 1930s, led by Ove Leijonhufvud, stripped away much of this later work to create the calmer, more restrained interior visitors see today. The altarpiece from this restoration incorporates two seventeenth-century paintings that may have belonged to the church's original furnishings. Among the fittings, the font dates from 1643 and is the work of Jost Schütz, who created much of the church's original interior decoration, while the pulpit, added in 1828, carries reliefs symbolising the sacraments and commandments.
Sankt Jacobs kyrka has long been associated with Swedish choral and organ music, serving for much of the twentieth century as a base for musicians who shaped the wider national musical scene, including figures later linked with the Royal Opera and prominent choral conductors. Its organ history is notably complex, with instruments built, rebuilt and enlarged across several centuries, culminating in a substantial new organ installed behind the historic eighteenth-century case in the 1970s.
The church ceased to be an independent parish in 1989 and its last regular Sunday service was held in 2012, after which it began to be used for concerts, meditation, teaching and pilgrimage activities. It was closed for renovation from 2024 and reopened in late 2025, though visitors should check current access separately rather than relying on this history.