Although it is only 3 miles from Charlbury, the tiny hamlet of Shorthampton remains out of the way and little known. The tiny church is situated on sloping ground looking out over the Evenlode valley, close to a cluster of farm buildings. When it was built in the late C12th, it probably had a single-cell plan. Early in the C14th a chancel was added, and later the nave was widened on the S side. Subsequently, apart from moving and inserting windows, doors and squints, and adding a bell-cote, there were no further structural changes. Romanesque features include a round-headed window in the N nave wall, a blocked round-headed doorway on the W wall, and a tub font.

The church belongs to the ancient parish of Charlbury with Shorthampton, a title surviving from when the minster church at Charlbury had a number of churches under its wing. It is first referred to in a document of 1296. While the other churches all gradually gained independence, Shorthampton was too small to separate. As the mother church came under the patronage of the Benedictine abbey of Eynsham, the latter is thought to have been responsible for building the chapel at Shorthampton, and also at nearby Chadlington (VCH).

The church is best-known for its wall paintings, uncovered in 1903 and recently restored, that probably span five centuries.

The doorway mounted on the W wall is believed to have been moved to this location from the centre of the N nave wall in the C18th to give access to a W gallery. Inside, a recessed shallow arch marks its probable original site. The doorway was later filled in when the W gallery was removed.