Finnart was no amateur. He had toured Europe studying the new Italian style of artillery fortification, returned to Scotland as an accomplished engineer, and been appointed King's Master of Works. He oversaw the defenses at Blackness Castle and the Renaissance facades of Linlithgow Palace. Craignethan was his personal showcase, where his domestic and military talents could share a single site. The keep was modest, a low rectangular block 21 by 16 meters with rounded bartizans on its corners and decorative machicolations over the door. The serious defenses lay elsewhere. The west wall of the inner courtyard was up to 5 meters thick, designed specifically to absorb cannon fire from the higher ground that overlooked the castle, with the keep tucked behind it like a protected child. It was clever and expensive and never tested. In 1540 Finnart was executed for treason. Everything he had built passed to the crown.

The Hamiltons regained Craignethan two years later. Finnart's half-brother, James Hamilton, 2nd Earl of Arran, added the large outer courtyard and made the place a private royal residence in all but name. He was, after all, regent of Scotland during Mary, Queen of Scots's infancy, and he became Duke of Chatellerault. His household books record visits to Craignethan in March 1543 and January 1548, complete with notes on what was eaten. When Mary's reign fell apart, Arran's son Lord Claud Hamilton entertained the queen at Craignethan on the night before the Battle of Langside in 1568. She lost the battle, fled to England, and never returned. The Hamiltons surrendered Craignethan and Cadzow to the Regent Moray, who came in person on 15 May 1568 to receive the keys. They were not done. Lord Claud and his brother Lord John recaptured the castle by force later that year. In 1570, when Moray was assassinated in Linlithgow by a Hamilton, the family reaped what their feud had sown.

By 1579 the Hamiltons were outlawed and Lord Claud had fled to France. Royal artillery rolled toward Craignethan. Both Craignethan and the Hamilton stronghold at Cadzow offered to surrender on terms; the king's men refused. The House of Hamilton surrendered unconditionally on 18 May. The garrison at Craignethan abandoned the castle in the night rather than submit. By royal authority a young man named Sir James Hamilton of Libberton was sent to slight the castle, the technical term for deliberately rendering a fortress indefensible. He destroyed the northwest tower and the great 5-meter west wall, the inner barmkin that had been the heart of Finnart's defense scheme, tumbling its stones into the ditch. The whole point of the castle, the wall that had taken its designer to Italy and back, was thrown down.

Two and a half centuries later, Sir Walter Scott published Old Mortality, a novel of the Covenanter risings, partly set at a fictional fortress called Tillietudlem. Readers, looking for a real place, settled on Craignethan as their model, even though Scott protested that he hadn't been thinking of the castle when he wrote the book. He gracefully gave in: in 1830 he added a footnote acknowledging that Craignethan's ruins 'have something of the character' of his invented castle. In 1834 his son-in-law brought J. M. W. Turner to Craignethan; Turner sketched the castle from across the Nethan Gorge and made several drawings among the ruins. A railway station called Tillietudlem opened nearby in 1876, and the houses that grew up around it became the hamlet of Tillietudlem. A fictional name from a novel, drawn from a misunderstood Walter Scott footnote, became a real place on the Ordnance Survey map. Craignethan, slighted and unfinished, has been a more durable cultural force as ruin than it ever was as castle.