In 1489 his first cousin King James IV made him Sheriff of Lanark, a position his father had previously held, and a Scottish Privy Counsellor.

[1] Between April and August 1502, Hamilton commanded a naval fleet sent to help King Hans of Denmark, James IV's uncle, defeat a Swedish-Norwegian rebellion.

[1] In September 1507, James IV sent Hamilton as his ambassador on a diplomatic mission to the court of Louis XII of France.

When returning in early 1508, he was briefly detained in the Kingdom of England by Henry VII, who was suspicious of a renewal of the Auld Alliance between Scotland and France.

[1] During the minority of King James V, Hamilton opposed Archibald Douglas, 6th Earl of Angus and the English party.

The same year he led an expedition to the border to punish the murderers of the French knight Antoine d'Arces ("De la Bastie").

This award of divorce was repeated in 1510, suggesting that Hamilton had continued living with her, after 1504, and was held by some to undermine the dissolution of the first marriage as invalid.