The A1 (Great North Road) originally ran through the heart of the village, but during the 1980s a bypass was built to the East of the village. Ayton was the location of a coaching inn on the road between London and Edinburgh.
The splendid edifice of Ayton Castle, the caput of the Scottish feudal barony of Ayton, dominates the town and district. It is built around a peel tower, a stronghold of the Home family, which burnt down in 1834.
The estate was subsequently purchased by William Mitchell (later Mitchell-Innes) of Parsonsgreen, Edinburgh, Chief Cashier of the Royal Bank of Scotland. From 1846-51 James Gillespie Graham was commissioned to build a new castle at Ayton in the Scottish Baronial style in red sandstone. Further additions were made in the later 19th century. The interiors of the 1875 are still largely extant. William's son, Alexander Mitchell-Innes (1811–1886), commissioned James Maitland Wardrop to build Ayton Parish Church, with a 36-metre (118 ft) spire, and stained glass windows by Ballantine & Sons.
In 1895 the barony of Ayton was sold to Henry Liddell-Grainger of Middleton Hall, Northumberland. His descendant, Ian Liddell-Grainger MP, is the current feudal baron of Ayton, and proprietor of Ayton Castle.