In 1437, Henry VI (Henry V's son ) came of age and began to actively rule as king. To forge peace, he married French noblewoman Margaret of Anjou in 1445, as provided in the Treaty of Tours. Hostilities with France resumed in 1449. When England lost the Hundred Years' War in August 1453, Henry fell into mental breakdown until Christmas 1454.

Henry could not control the feuding nobles, and a series of civil wars known as the Wars of the Roses began, lasting from 1455 to 1485. Although the fighting was very sporadic and small, there was a general breakdown in the power of the Crown. The royal court and Parliament moved to Coventry, in the Lancastrian heartlands, which thus became the capital of England until 1461. Henry's cousin Edward, Duke of York, deposed Henry in 1461 to become Edward IV following a Lancastrian defeat at the Battle of Mortimer's Cross. Edward was later briefly expelled from the throne in 1470–1471 when Richard Neville, Earl of Warwick, brought Henry back to power. Six months later, Edward defeated and killed Warwick in battle and reclaimed the throne. Henry was imprisoned in the Tower of London and died there.

Edward died in 1483, only 40 years old, his reign having gone a little way to restoring the power of the Crown. His eldest son and heir Edward V, aged 12, could not succeed him because the king's brother, Richard III, Duke of Gloucester, declared Edward IV's marriage bigamous, making all his children illegitimate. Richard III was then declared king, and Edward V and his 10-year-old brother Richard were imprisoned in the Tower of London.

In summer 1485, Henry Tudor, the last Lancastrian male, returned from exile in France and landed in Wales. Henry then defeated and killed Richard III at Bosworth Field on 22 August, and was crowned Henry VII.