The village toponym is derived from the Old English for "farm at a narrow pass". The Domesday Book of 1086 records it as Dortone, and in the 13th century it was Durtone.[2]
The nave and chancel of the church building may be 12th century, as is the bowl of the font.[2] There is a 13th-century lancet window in the nave.[4] The south porch was added in the 13th century, es evidenced by a blocked window of that date in its east wall.[2] In the 14th century the Decorated Gothic south aisle was added, the chancel arch was at least partly rebuilt and the present east window and piscina were added.[2] The present stained glass in the east window is 15th century.[5] The present entrance arch to the porch was added in the 15th century, the base of the font is from the same century and the Perpendicular Gothic window in the south wall of the south aisle was added in about 1480.[2]
St. John's has three bells hung in a timber-framed bell-cot, plus a small Sanctus bell.[2] Bartholomew Atton of Buckingham cast the tenor bell in 1604 and Robert Atton cast the second bell in 1626.[2]John Taylor and Sons cast the treble bell in 1828,[2] presumably at the bell-foundry they then had at Oxford.