In 1012, according to the Annals of Clonmacnoise, a single thunderbolt reduced the entire town of Kildare to ash, sparing just one house. It is a peculiarly vivid detail, and it tells us something easily overlooked: by the early eleventh century, what had begun as a monastic enclosure had already grown into a recognisable urban settlement, dense enough for the destruction of almost all of it to be worth recording. The town sits on a low ridge at the western edge of the Curragh, the great open plain of County Kildare, and its name comes from the Irish Cill Dara, meaning 'the church of the oak', a reference to a tree that the seventh-century writer Cogitosus described as standing beside St. Brigid's monastery, founded in the early sixth century.

The Norman period transformed the settlement decisively. A borough was established before 1176, becoming the principal manor of Strongbow's lordship in north Leinster, with the earliest fortification likely a motte, the earthen mound typical of early Anglo-Norman defence. By the close of the thirteenth century the town held a castle, a cathedral, and both Franciscan and Carmelite friaries, and in 1309 to 1310 a parliament convened there. In 1316, John Fitzthomas, newly created earl of Kildare, received the town and castle by grant, and estimates suggest the population stood at around 1,000 at that time. In 1515 a new charter brought a weekly market and permission to enclose the town with walls and a fosse, the defensive ditch that would run along the perimeter. Then the Nine Years War arrived. In 1598 Kildare was so heavily damaged during an engagement that the traveller and writer Fynes Moryson described it as 'altogether disinhabited'. The cathedral was roofless by 1604; properties throughout the town were recorded in 1607 as 'ruinous' or 'lately burned'. The town recovered enough to serve as a garrison during the Confederate War of 1641 to 1653, but a census taken around 1659 counted only 359 people, a long way from the medieval borough at its height.