The name derives from popel (pebble) and tun (hamlet, farm), probably meaning "farmstead on pebbly soil". The village is mentioned in the Domesday Book and was owned by the Archbishops of York. It received its charter from Archbishop Oswald in 972. Nether Poppleton used to be referred to as "Water Poppleton" whereas Upper Poppleton was "Land Poppleton".
St. Everilda's Church is named after a 7th century Saxon saint, one of only two churches in Britain to be named so. Everilda established a convent at Everingham, East Riding of Yorkshire where there are St. Everilda's (Church of England) and St. Mary's and St. Everilda's (Roman Catholic).
After the church, Nether Poppleton Tithebarn is the oldest building in both the Poppletons. It has associations with Prince Rupert of the Rhine.