He first appears on record on a charter of 1426, granting him the rights to the lands of Dalserf, which had been alienated by his father.

This charter raised all his estates into the entail of that rank, with its Capital Messuage at the Orchard, (later Hamilton Palace), at Cadzow.

He was back in Scotland by February 1455 at which time Hamilton and the Earl of Douglas's brothers ravaged and burned much of Lanarkshire.

As recompense for his Volte-Face, Hamilton was created Sheriff of Lanark, in July 1455, and certain of the Earl of Douglas' forfeited lands were made over to him.

Hamilton was made Bailie of the Priory of Lesmahagow, a Douglas foundation, and was granted the privilege of the lands of Finnart.

Hamilton married firstly, in 1406, Lady Euphemia Graham (died 1468), daughter of Patrick Graham, de jure Earl of Strathearn and Euphemia Stewart, Countess of Strathearn and widow of Archibald Douglas, 5th Earl of Douglas.

His grandson, James Hamilton, notably served as Sheriff of Perthshire, and his descendants became the Lords Belhaven and Stenton.

Another illegitimate child by Janet Calderwood was David Hamilton, Bishop of Argyll and commendator of Dryburgh Abbey.