Rhuddlan first appears in recorded history in the last years of the eighth century, when there was no town of Rhyl and the shore road from Prestatyn to Abergele did not exist. Instead, the Clwyd and the marshes off its estuary, now reclaimed and drained and cultivated, formed a natural barrier athwart the coastal approach to the mountainous heart of North Wales. The settlement of Rhuddlan is likely to have owed its origin to the presence at this point, from very early times, of the lowest fording-place on the river, from which a track led across the marsh to Vaynol and beyond. Its position thus marked it out as a key point in the racial struggles which for some 600 years (c.700-c.1300) swayed to and fro across the Welsh and English border.
The castle came under attack in the Welsh rising of 1294, and again in the Glyndwr rising of 1400, when the town was badly damaged but the castle held out. Rhuddlan was in Royalist hands during the Civil War, until forced to capitulate in 1646. In 1648 it was partially demolished to prevent its further use.