Upninkai were first mentioned in 1442 in the will of Kristinas Astikas who has been the first known lord of Upninkai lands. His son Radvila Astikas built the first church here before 1477. It was held by the Reformers from the late 16th century until 1650. The present Neoclassical Roman Catholic church of Archangel Michael was constructed in 1845 north of the town, on left bank of Šventoji River flowing nearby the town. It was set up in the former manor's masonry granary and has been improved later on.