In ancient times, Manister was known as Kilmargy. According to the civil survey of 1654, Clochnamanagh (now in the neighbouring parish of Fedamore) was at that stage part of Manister, while Kilonehan was still a separate parish. Today Kilonehan is part of Manister parish.

In 1704 Bruff had part of the parish of Manister, Tullybracky. Manister formed part of the union of parishes of Bruff and Fedamore until the mid nineteenth century. The parishes of Fedamore and Manister were united at the beginning of the 18th century. They were separated to become individual parishes in 1858. The name Manister comes from the Irish An Mhainister meaning 'the abbey'. According to a local history written by David Cantwell, native of the parish, the monastic lands, which belonged to Monasteranenagh, were to form the parish of Manister, much as it is in area and boundaries today.

The Colleen Bawn grew up in her uncle's house in Manister. Her real name was Eileen Hanley. She was lured away by Lieutenant John Scanlan of the Royal Navy. A mock marriage took place in 1819. Soon after, she was drowned in the Shannon River in Glin. Scanlan and Stephen O'Sullivan, a Glin man, were hanged for her murder.

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