Although the present house of Manderston dates to the early 20th century and incorporates a Georgian mansion, it is built on the site of an old tower house.

In the 16th century Manderston was owned by the Home family, and later, briefly, by the Swinton family.

Around 1790 a new house was built for Dalhousie Watherston, which may have entirely replaced or incorporated the old tower house. Between 1901 and 1903 the then owner, Sir James Miller, commissioned the architect John Kinross to completely rebuild the house at any expense.