The current St Peter's on Aungier Street was built between 1863 and 1867, but the ground it occupies has been a place of Christian worship for considerably longer than that, possibly stretching back before the Norse settlers who shaped early Dublin. Researchers have identified it as the strongest candidate among the medieval churches on the south side of the city to represent a pre-Norse foundation, which would place its origins somewhere in the early Christian period of Ireland, before the ninth century and the arrival of Scandinavian settlers.

The church's full medieval name, St Peter's de la Hulle, is itself a clue to its age, a Latin-French hybrid pointing to a hilltop site that was already established when the Anglo-Normans arrived and reorganised Dublin's ecclesiastical geography. It was listed among the possessions of Holy Trinity in a papal bull issued by Pope Alexander III in 1179, and it functioned as one of the original parochial churches of Anglo-Norman Dublin. By 1370, however, the building had fallen into severe neglect; contemporary documents described it as ruined to its foundations, and a papal indulgence of one year and forty days was granted to those who contributed to its repair. An indulgence of this kind was a standard medieval mechanism for fundraising, offering a reduction of time in purgatory in exchange for charitable works. The site was eventually rebuilt more substantially when Francis Aungier donated the land in 1680 for a T-shaped church with a north transept and galleries. The present building replaced that structure during the 1860s.

Excavations carried out in 1999 uncovered paving tiles and 69 burials beneath the site, physical evidence of the long human activity concentrated here across many centuries. The church itself sits on Aungier Street in Dublin's south city, a busy thoroughfare that can make it easy to pass without a second glance. The street was named after the same Francis Aungier whose donation shaped the site's post-medieval history. Visitors who do pause will find a Victorian building unremarkable from the outside, but the excavation record and the documentary trail running back to 1179, and arguably much further, give the site a quiet depth that its surroundings do nothing to advertise.