Construction of Denbigh Castle and the town walls began in 1282. The Burgess Gate, whose twin towers still appear on the town's civic seal, was once the main entrance. The fortress was a key piece of Edward I's strategy for locking down North Wales after his conquest - a chain of new castles at Conwy, Caernarfon, Harlech, Beaumaris, and here in the Vale of Clwyd. The Welsh did not accept the conquest quietly. In 1294 Madog ap Llywelyn led a major rising. Denbigh's castle was captured by the Welsh in autumn, and on 11 November 1294 an English relief force was defeated by the rebels. Edward I himself retook the town that December. A century later, in 1400, Denbigh was burned again in the rising of Owain Glyndwr - the great Welsh rebellion that for a few years made Glyndwr the de facto Prince of Wales. The town within the walls was largely destroyed in the Wars of the Roses (1455-1487). The settlement shifted outside the old walls to the north-east, centred on a market place along the High Street where Denbigh still trades.

In 1579 Robert Dudley, 1st Earl of Leicester - Queen Elizabeth I's favourite, soldier, courtier, would-be husband, the man who built Kenilworth Castle for her - was also Baron of Denbigh. He decided the town deserved a cathedral. Denbigh would replace neighbouring St Asaph as the diocesan city; Leicester would fund a great new church. Work began. Then the money ran out. Then Leicester died in 1588. The project was abandoned with only the walls and parts of the structure built. Leicester's Church - still called that today - sits as a roofless shell in the care of Cadw, the Welsh historic monuments body. The roofless arcades, the half-finished towers, the empty windows looking out over the Vale of Clwyd: the building is one of the more melancholy ruins in Wales, a monument to a courtier's ambition that died with him. The County Hall - now the town library - was built in 1572 to serve as the market hall and courthouse for when the Denbighshire courts sat in Denbigh, which was the county town when the new shire was created in 1536.

Henry Morton Stanley was born in Denbigh in 1841 as John Rowlands, the illegitimate son of a teenage mother. He spent his childhood in St Asaph workhouse before emigrating to America, taking the name of a New Orleans merchant who briefly fostered him, and reinventing himself entirely. He fought on both sides of the American Civil War. He became a journalist for the New York Herald. In 1871 the paper sent him to Africa to find the missing missionary-explorer David Livingstone. When Stanley found him at Ujiji on the shore of Lake Tanganyika, the greeting he later said he had used - 'Doctor Livingstone, I presume?' - became the most famous sentence in 19th-century journalism. Stanley went on to map the Congo basin, became a key figure in the brutal Belgian colonisation of central Africa, and is now a deeply controversial figure. Beatrix Potter spent her childhood summers at Gwaenynog Hall just outside Denbigh between 1895 and 1913, staying with her uncle and aunt. The Hall's walled vegetable garden was the direct inspiration for the garden in The Tale of the Flopsy Bunnies. Other Denbigh children: Kate Roberts, the great 20th-century Welsh-language novelist; Twm o'r Nant (Thomas Edwards), the 18th-century playwright whose theatre still operates in the town under his name; the cartographer Humphrey Llwyd; and CDawgVA, the YouTuber and podcaster, born 1996, presenter of Trash Taste.

For over fifty years Denbigh has held a barrel-rolling competition on Boxing Day in the town square, an unselfconscious midwinter ritual that draws spectators in from the surrounding villages. Denbigh Cricket Club, founded in 1844, is one of the oldest in Wales. Denbigh Castle and town walls, Leicester's Church, St Marcella's medieval parish church, Theatr Twm o'r Nant, and the Cae Dai 1950s museum draw visitors year-round. But the most haunting building in the town is the North Wales Hospital, established in the 1840s for the treatment of psychiatric illness. For a century and a half it was the town's largest employer. It closed in 1995 and has fallen into disrepair since. In 2008 a special series of the paranormal television programme Most Haunted, titled Village of the Damned, was filmed there over seven days. In 2018 the derelict site passed to Denbighshire County Council. The Most Haunted episodes were entertainment; the actual North Wales Hospital - thousands of patients across 150 years, an institution that defined how mental illness was treated in north-east Wales - is a more serious place than the television cameras suggested.