Located next to the Lindenhof hill, site of the former Roman castle, it was built on the site of a temple to Iuppiter. An early church of 10 by 7 metres is archaeologically attested for the 8th or 9th century. This building was replaced by an early romanesque church around AD 1000, in turn replaced in 1230 by a late romanesque structure, parts of which survive. Rudolf Brun, first independent mayor of the town, was buried here in 1360. The nave was rebuilt in 1460 in Gothic style. Prior to the reformation, St. Peter was the only parish church of the town, the rest being part of monasteries.
The current building was consecrated in 1706 as the first church built under Protestant rule. Until 1911, the steeple was manned by a fire watch. Restoration work was carried out in 1970 to 1975. The steeple's clock face has a diameter of 8.7 m, the largest church clock face in Europe. The bells date to 1880.
Peculiarly, the church's steeple is owned by the city of Zürich, while the nave is owned by the St. Peter parish of the Swiss Reformed Church.