The church was built around the turn of the fourteenth century, and it is thought it may have been consecrated in 1302, the year Archbishop Nils Allesson is recorded as visiting the parish. Unusually for the region, Ärentuna kyrka is not a hall church: its chancel is noticeably narrower than the nave, giving the building a more traditional, elongated profile than many neighbouring Uppland churches.
The walls are decorated with lime-plaster paintings from two distinct periods. Fourteenth-century decorative borders with plant motifs survive alongside more elaborate images of saints and ornamental scenes painted in the 1440s by an artist known only as the Ärentuna Master. The subject matter, including scenes from the lives of saints and the Creation narrative, is said to reflect a Franciscan tradition of religious imagery.
The chancel's original wooden barrel vault was replaced with a brick cross-vault before the church's reconsecration in 1435; remnants of the old wooden vault were later found hidden in the ceiling during restoration work and are partly preserved at the Historical Museum. A small spired bell-turret once stood on the nave roof, visible in a seventeenth-century drawing, before being removed in the eighteenth century. A porch was added on the south side, likely at the time the brick vaulting was installed, and the windows were enlarged in 1788. A major restoration between 1960 and 1967 uncovered further paintings on the west wall and saw the old organ gallery removed and a new organ installed. A detached wooden bell tower stands east of the churchyard wall, and a stepped stile gate survives in the eastern churchyard wall.
Among the furnishings is a Madonna shrine dating from the 1470s, and a fragment of a medieval font remains in the porch. A stained-glass window depicting the Good Shepherd, made by the artist Gunnar Torhamn in 1928, decorates the chancel. According to an uncertain tradition, the so-called Ärentuna Madonna once stood in the church, though it has long been part of Uppsala University's art collections and is now displayed at the Gustavianum museum.