The fuller Irish form, Daingean Uí Chúis, translates roughly as "the fastness of O'Cuis or O'Hussey", though the Ui Cuis family are otherwise unknown to history, and the earliest written record of the extended name, appearing in 1322 as "Dengenyhonysh", actually predates the known involvement of the Hussey family in the town by some margin. It is a place whose identity rests on a foundation of productive uncertainty.

The town appears to have been an Anglo-Norman creation, planted on what was likely virgin ground sometime before 1278-9, when customs returns first place it on record as a functioning port. By 1299 the community was organised enough to be collectively fined for the escape of one Walter Laundrey. The cantred, a medieval administrative land division, passed through several hands: from a grant to Robert son of Geoffrey de Marisco around 1216, to his daughter Christiania, who sold it to Sir Maurice FitzMaurice, and eventually to Thomas de Clare, who held it by the early fourteenth century. The harbour was the town's reason for existence, sheltered behind a ridge of high ground that cuts across the mouth of the bay and buffered on the landward side by a crescent of mountains. Dingle and Tralee were significant enough in the late thirteenth and fourteenth centuries to serve as centres for royal customs collection, though Dingle was probably never more than a minor port by broader standards. What it lacked in scale it compensated for in persistence, surviving repeated destruction. Diarmait MacCarthaig burned the town in 1316. James FitzMaurice landed with six Spanish ships in 1579 and burned it again; contemporary accounts described it as "wholly sacked", "razed", and "broken". By 1580 most inhabitants had fled. Then in 1582 the earl of Desmond besieged what remained, and an English traveller writing in 1589 recorded that only four houses in the entire town had held out against him, their occupants fortifying themselves and refusing to yield. In 1598, James FitzThomas, known as the "sugan" earl, a claimant to the Desmond title whose nickname derived from the Irish word for a straw rope, landed at Dingle with some two thousand Spaniards and the town surrendered to him. Then in 1645 a parliamentarian force under Captain Robert Moulton pillaged and burned it again. The town's formal charter of incorporation, first proposed in 1585 to help restore its "ruinous and decayed estate", was apparently not formally granted until 1606, though references to a portreeve suggest some form of civic organisation existed earlier still.