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Downpatrick is one of Ireland's most ancient and historic towns. It takes its name from a dún (fort), which once stood on the hill that dominates the town and on which Down Cathedral stands.
Ptolemy, about the year AD 130, includes it (in Latin) as Dunum in his list of towns of Ireland. The old name of the town was Rath Celtair named after the mythological warrior of Ulster called Celtchar (in modern Irish: Cealtachair) who resided there and who fought alongside Ulster King Conchobar mac Neasa (anglicised Conor Mac Nessa) and is mentioned in the Ulster Cycle and, in particular, the Táin Bó Cuailgne. The name was superseded by the name Dún Lethglaise then Dún Dá Lethglas which in turn gave way, in the 13th century, to the present name of Dún Phádraig (anglicised as Downpatrick) – from the town's connection with the patron saint of Ireland.
Saint Patrick was buried here in 461 on Cathedral Hill, together with Saint Bridget an Saint Columkille, within the grounds of Down Cathedral (before its construction). His grave is still a place of pilgrimage on St Patricks Day (17 March each year). The Saint Patrick Visitor Centre in Downpatrick is purpose-built to tell the story of St Patrick.
From the seventh century the dominant power in Ulster were the Dál Fiatach so much so that the title "Rí Uladh" could simultaneously mean "King of Ulster" and "King of the Dál Fiatach". County Down was the ancient centre of the Dál Fiatach lands, and the chief royal site and religious centre of the Dál Fiatach was at Downpatrick from where they ruled Ulster for centuries.
In 1137, St. Malachy after resigning as Archbishop of Armagh, separating the two dioceses and appointing another as Bishop of Connor, became the Bishop of Down. He administered the diocese of Dún dá leth glas (Down) from Bangor and introduced a community of Augustinians (canons) to Dún dá leth glas dedicated to St. John the Evangelist and repaired and enlarged Down Cathedral.
After having received a grant of Ulster from King Henry II of England, Norman Knight, John de Courcy set out from Dublin in early 1177 to take possession of it. He marched north to with a force of 20 knights and 300 men and reached Downpatrick four days later. Downpatrick was an open ecclesiastical town of the old type and the invaders rode in and surprised it in the small hours of 2 February. De Courcy attacked the fortress and administrative centre of Rath Celtair (the Mound of Down), defeating and driving off Rory MacDonlevy (Ruaidhri Mac Duinnshleibhe), King of the Dál Fiatach and Ulster (Ulaid).
In 1183, John de Courcy brought in some Benedictines from the abbey of St. Werburgh in Chester (today Chester Cathedral) in England and built a cathedral friary for them at Downpatrick. This building was destroyed by an earthquake in 1245. De Courcy reputedly found not only the bones of St. Patrick on Cathedral Hill but also the bones of St. Brigid and St. Colmcille (St.Columba) and in the presence of the Papal Legate, Vivian, Cardinal-priest of Santo Stefano Rotondo (also Santo Stefano al Monte Celio), the relics were reburied on 9 June 1186.
In 1260 Brian O'Neill (Brian Ua Néill), King of Tír Eoghain (Tyrone) and who had been acknowledged as High King of Ireland by Hugh O'Conor of Connacht and Tadhg O'Brien of Thomond marched to Downpatrick, a centre of English settlement, and, allied with a Connacht force under Hugh O'Conor, fought the foreigners in the Battle of Down. The battle took place outside the city of Down and O'Neill, 8 Connacht lords and many others died. The death of Brian O'Neill and the defeat of the Irish was lamented by the Cenél nEógain bard Gilbride MacNamee (Giolla Brighde Mac Con Midhe)(1210–1272) in a poem.
Following the rebellion of Shane O'Neill in 1567, Downpatrick fell briefly into Irish hands before being re-taken by Sir Richard Morrison (Moryson).
Great scholar, poet, bishop and Franciscan theologian Aodh Mac Aingil (real name Aodh Mac Cathmhaoil) was born outside Dún (Downpatrick) in 1571.
On 21 January 1575, three Franciscans John Lochran, Donagh O'Rorke, and Edmund Fitzsimon were hanged at Downpatrick.