For centuries the illuminated gospel manuscript, probably produced on the island of Iona around 800 AD, sat on the altar of a parish church in a County Meath market town before being removed to Dublin in 1653. That town, Kells, was itself something considerably more than a convenient resting place for a famous object. It occupied the slopes of a low hill east of the Hill of Lloyd, and long before it became a monastery it was known in Old and Middle Irish sources as Ceanannas na Rí, meaning roughly 'white-headed stronghold of the kings', reputedly a fortified seat of Diarmait Mac Cerbhill, King of the southern Uí Néill, who died in 565 AD. Prehistoric artefacts recovered across the site suggest the settlement is older still.

The monastic phase began when the community of Iona, fleeing some of the earliest Viking raids recorded in Britain or Ireland, relocated here around 800 AD. The principal church was built by 814, the relics of St Columba were eventually brought to Kells, and the town became the head of the Columban familia, the network of monasteries associated with the saint, until around 1150. Its ecclesiastical enclosure measured roughly 280 metres by 350 metres, and the settlement functioned as a significant metal-working centre; the shrines known as the Cathach and the Misach were both made here. Despite repeated attacks by Viking forces and Irish war-bands through the tenth to twelfth centuries, and a raid led by Dermot McMurrough as late as 1170, the place remained consequential enough to host a major reforming Church synod in 1152. The Anglo-Norman lord Hugh de Lacy made Kells the caput, or administrative centre, of a manor before 1176, and his son Walter granted it a borough charter sometime after 1194. By 1211 the town had lost its episcopal status to Trim, and its monastery was converted into a parish church. It sat on the edge of the Pale, the zone of English colonial control in medieval Ireland, and a section of the Pale ditch survives about three kilometres to the northwest. A murage grant, the royal licence that allowed a town to levy tolls for the upkeep of its walls, was first issued here in 1326. In 1598 Kells was still counted among the four walled towns of Meath.

The medieval walls have almost entirely disappeared, but their circuit can be traced through the property boundaries recorded in a 1663 valuation and on Down Survey maps from the 1650s, running from Canon Gate across the Fair Green to Carrick Gate, along the back of Carrick Street to Maudlin Gate, and so on through what are now Headfort Place, Bective Street, and Suffolk Street, enclosing roughly 20 hectares in all. One mural tower survives. What remains above ground at the monastic core is more legible: St Columba's House, a round tower, three high crosses, and the site of the parish church still occupy the graveyard. The site of St John's friary lies in a separate graveyard on the Navan Road, where a number of medieval graveslabs can also be found.