Longford is a quiet exception. There is no evidence of any Anglo-Norman hand in its founding; it grew instead from a native Irish stronghold at a fording point on the Camlin River, its very name derived from the Irish 'longphort', meaning fortress. That origin gave the settlement, and eventually the county, its name, and it placed Longford in a small and rarely acknowledged category of Irish urban centres whose development was entirely Gaelic in character.

The O'Farrells, the ruling family of Anghaile, were the driving force behind its early growth. In 1400 they established a Dominican priory on the north side of the river, and by 1445 Longford had become the seat of the O Fearghail of lower Anghaile following a division of the territory. By 1448 it appears in the Annals of the Four Masters as 'Longphort Ui Fergail'. A native Irish market had developed by the late fifteenth century, drawing merchants from the east coast and attracting the pointed attention of the Irish parliament, which moved to forbid English merchants from trading there, viewing it as damaging competition for the English markets of Meath. The O'Farrells held the settlement until the reign of Elizabeth I, by which point the place had become significant enough that when the surrounding territory was formally shired in 1571, the new county simply took its name. The town's formal reinvention as an English colonial project came in stages: a royal market grant issued to Richard Nugent, baron of Delvin, in 1605 was never acted upon, and as late as 1613 there was said to be in the county 'no town fit for it' to send burgesses to the Irish Parliament. A fresh grant followed in 1620 to Francis Aungier, baron of Longford, authorising a manor, a market, and two fairs. In 1666 Irish forces under Cornet Nangle attacked the town and burnt most of the English houses, conspicuously leaving the Irish ones standing. Two years later, Charles II incorporated it as a borough.

Writing in 1682, a commentator named Nicholas Dowdall described Longford as a 'Large Countrey Village having but few good houses in it', noting a small river of limited use beyond driving a few mills, a Dominican abbey, and a stone bridge lately built. That picture of modest, slightly dishevelled functionality is legible still in the town's layout. The area around Bridge Street and Church Street preserves what is likely the oldest urban fabric, corresponding to the late sixteenth century, while the long, narrow burgage plots fronting Main Street, a form of medieval land division allocated to town tenants, suggest the seventeenth-century phase of development. A market-house, a gaol, a market cross, and two seventeenth-century houses are also associated with this period of the town's formation.