Both clans were one time allies but changing allegiances create a power struggle between them which continued on and off until the Battle of Slieve-na-Aura in 1583. This confrontation redefined the power structure in Ulster and Dunluce became the main MacDonnell castle along the north coast. Hugh MacFelim O'Neill, Rory MacQuillan and Captain Thomas Chatterson were killed at the battle which had been planned by them to remove the MacDonnell's. Sorley Boy MacDonnell knowing the glens well had made his way at night up through Glendun and positioned his forces on firm ground surrounded by bogland which they covered with rushes. When the horses and foot soldiers charged they ended up in the boggy ground and became easy victims to the lighter equipped MacDonnells.

A traditional local saying goes - 'There's been nobody fooled by a rush bush but a MacQuillan'. There are references to Sorley Boy MacDonnell flying, much to the displeasure of Queen Elizabeth 1st, a battle standard captured after a skirmish with the English, he is also reputed to have mounted four cannons salvaged from the Girona along the castle walls. The Girona was a galleass of the Spanish Armada which foundered on Lacada Point at the Giant's Causeway in 1588, local folklore tells of victims being buried in St. Cuthbert's graveyard in nearby Dunluce Castle. The MacDonnell's held a 'St Columcille Cross' named after the Irish saint, this was taken along with other valuables by Sir John Perrott who took the castle on instructions from Queen Elizabeth in 1584.

There were said to have been tapestries and exquisite curtains including a set which had belonged to Cardinal Wolsley at Hampton Court. The inventory lists six sets of chairs of state, which would have been placed under an elaborate canopy. Sixty other elaborately upholstered chairs and stools and a library of books. There were saddles worked with gold and silver, finely inlaid cabinets and valuable objects such as telescopes, celestial and terrestrial globes. The most valuable listings are the priests vestments.  The Countess is credited with renovating St. Cuthbert's Church (nearby to the castle) it was originally thatched and is recorded as having a lavish interior which included the signs of the zodiac painted in the ceiling plaster.

In 1639, while the Earl and his Countess were at home, part of the castle fell into sea, a significant part of the castle directly above the entrance to the mermaid's cave and with exceptional views over the ocean, stories that it was the kitchen may be slightly exaggerates as the kitchen still exist within the ruins, the vanished rooms may have been guests or summer rooms used by the occupants. The 1641 rebellion saw the castle besieged by an Irish army, the surrounding village was burnt, the castle held out under the command of a Captain Digsby and was relieved by the Earl.  Most of the Scottish settlers and merchants escaped to Scotland before the village was destroyed by fire.

Oliver Plunkett, the Archbishop of Armagh who had been recently canonized, was a visitor and described it as a 'palace washed on all sides by the sea'. The Battle of the Boyne in 1690 had repercussions for the MacDonnells who had supported the cause of the deposed King James II. Dunluce Castle was abandoned and  Ballymagarry House nearby became the Earl's main residence, part of its structure and garden walls are still standing. A barn survives with massive oak beams said to have come from Dunluce Castle after it was deserted.  Ballymagarry was destroyed by a fire in 1745 after which Glenarm Castle became the principal seat of the Earl of Antrim and the MacDonnell clan.