Prestbury is listed in the Domesday Book of 1086 as "Presteberie", part of the property of the church of Hereford, with 18 villagers, five smallholders, a priest, a riding man and 11 slaves.

In the middle of the 18th century a mineral spring was discovered in the parish, and by 1751 a local landowner, Lord Craven, had a business providing bathing and lodging.

The village is home to Prestbury Park, the Cheltenham Racecourse, which holds the Gold Cup race each March.

Notable Nicholson apprentices include Pat Eddery, Walter Swinburn, and Mouse Morris the 2006 Cheltenham Gold Cup winning trainer with the horse War of Attrition.

The parish is presently split between four wards of the Borough of Cheltenham: Swindon Village, Prestbury, Pittville (a very small part) and Oakley; three electoral divisions of the county of Gloucestershire: St Paul's and Swindon, Pittville and Prestbury, and All Saints and Oakley; and two parliamentary constituencies: Tewkesbury and Cheltenham.