For centuries Highlanders came to Crieff to sell their black cattle, whose meat and hides were sought by the growing urban populations of Lowland Scotland and the north of England. The town acted as the gathering point. In October 1714, Rob Roy MacGregor and his followers came down for the Tryst, marched to Crieff Town Square, sang Jacobite songs in front of the crowd, and drank loyal toasts to their uncrowned King James VIII. Two years later the same crowd came back as defeated rebels and burned the town. In 1731 James Drummond, 3rd Duke of Perth, laid out James Square at the centre and established a flax factory, trying to give the town an industry that did not depend on the price of beef.

In the 1745 rising the Highlanders wanted to fire the town again, reportedly saying she should be a braw toun gin she haed anither sing. The Duke of Perth, a friend of Prince Charles Edward Stuart, talked them out of it. In February 1746 the Jacobite army was quartered around Crieff, and Charles himself held his final war council in the old Drummond Arms Inn in James Square, behind what is now an abandoned hotel building on Hill Street. From here the prince and his commanders made decisions that would soon end at Culloden. Crieff survived this rising intact. The hangings, by contrast, happened at the bottom of Burrell Street, in an area called Gallowhaugh, where a wooden gallows had replaced an older hanging tree used by the Earls of Strathearn.

In the 19th century Crieff reinvented itself as a fashionable Highland destination. Wealthy Edinburgh and Glasgow businessmen built country retreats here. Many of them came for the hydropathic establishment, opened in 1868, which still operates as the Crieff Hydro. Crieff Town Hall was completed in 1850. The Crieff Junction Railway opened a station in 1856, linking the town to Perth, Comrie and Gleneagles, and bringing the Victorian tourist economy with it. The railway was killed off by the Beeching cuts in 1964, but the Hydro is still there, and so are several of the larger Victorian villas around its edges.

Modern Crieff is known for whisky and glass. The Glenturret Distillery, just north of the town, claims to be one of Scotland's oldest working distilleries. The Caithness Glass Visitor Centre brings tourists in to watch glass being blown. A few miles south-east stands Innerpeffray Library, founded around 1680, the oldest lending library in Scotland and still open to readers. Beside it, St Mary's Chapel dates from 1508. The poet William McGonagall, almost universally agreed to be one of the worst poets ever to write in English, immortalised the town with a couplet that reads as he intended: Ye lovers of the picturesque, if ye wish to drown your grief, take my advice, and visit the ancient town of Crieff.

Ewan McGregor was born here in 1971. His uncle is the actor Denis Lawson, who grew up in Crieff and was for a long time the more famous of the two. Neil Paterson, who lived in Crieff until his death in 1995, won the Oscar for Best Adapted Screenplay for Room at the Top. David Jacks, the first commercial producer of Monterey Jack cheese, came from Crieff; the Californian cheese is named after the immigrant who packaged it. William Reid, who died in Crieff in 2001, won the Victoria Cross in the Second World War for flying a damaged bomber on through the raid after being seriously wounded. For a market town of around 7,000 people, Crieff has produced an unusual quantity of consequential people.