The house was built in 1622, and was the home of the Foulis Baronets of Colinton. Sir James Foulis, 2nd Baronet, served as Lord Justice Clerk from 1684 to 1688, taking the title Lord Colinton. Bonnington later passed to the Wilkies of Ormiston. It was said to have been doubled in size in 1720, but the physical evidence of flues and fireplaces does not support this.
In 1858 the house was completely remodelled in a Jacobean style.  The house and its 100-acre (40 ha) estate was bought by the present owners in 1999, and in 2001 the house was refurbished by Lee Boyd Architects. Two new wings were designed by Benjamin Tindall Architects, granted planning consent in 2010 and completed in 2015. The grounds of the house have been developed as a sculpture park, now open to the public as Jupiter Artland.
- "Bonnington House: Listed Building Report". Historic Scotland.
- "Bonnington House". CANMORE. Royal Commission on the Ancient and Historical Monuments of Scotland.
- Buildings of Scotland: Lothian by Colin McWilliam
- "Story". Jupiter Artland. Retrieved 11 January 2013.
- "Appeal Decision Notice" (PDF). Directorate for Planning and Environmental Appeals. 5 October 2010.
- Ratho Village History, with pictures of Bonnington House