After the War of the Roses, the castle settled in royal hands on the execution of Sir William Stanley in 1495. The south range was partially rebuilt in 1529, reusing stone from earlier work. The old hall was subdivided and new living accommodation provided to its west. In 1563, the castle was granted to Elizabeth I's favorite, Robert Dudley, soon created earl of Leicester and Baron Denbigh, who held it as part of his extensive north Wales properties until his death in 1588. He may have reroofed it and added some of the square windows.
The castle was purchased in 1595 for about L5,000 by Sir Thomas Myddelton, a son of the governor of Denbigh Castle and successful London merchant. As a founder of the East India Company, an investor in the expeditions of Drake, Raleigh and Hawkins, he had the means to convert Chirk into a comfortable Tudor residence. His new stone north range contained a hall, buttery and kitchen, with upstairs drawing and dining rooms. This range, with alterations, became the main living quarters of the castle, while the old south range was gradually given over to servants.