Henry VI inherited the English crown in 1422 before his first birthday, and his father's claim to France passed to him soon afterward. Government initially rested with councils and senior relatives. He was crowned in England in 1429 and in Paris in 1431, but French resistance under Charles VII steadily undermined the projected dual monarchy. Normandy was lost in 1450, and defeat at Castillon in 1453 ended most remaining English rule in France.

Henry's personal kingship emphasized piety, peace, and patronage of education. He founded Eton College in 1440 and King's College, Cambridge, in 1441, endowing institutions intended to combine learning with religious observance. His marriage to Margaret of Anjou in 1445 supported efforts to settle the French war, but concessions and military reverses discredited royal advisers. Financial weakness and rival aristocratic networks further damaged the government's authority.

A serious episode of incapacity beginning in 1453 left Henry unable to conduct government. Richard, Duke of York, became protector, intensifying an existing struggle over access to power. Henry recovered, but violence between rival factions developed into the Wars of the Roses. His queen defended their son's succession while Yorkist opponents increasingly challenged the dynasty itself. Following the Yorkist victory at Towton in 1461, Edward IV took the throne and Henry fled.

Captured in 1465, Henry was confined in the Tower of London. An alliance between Margaret and the Earl of Warwick briefly restored him in 1470, although effective power lay with those managing the restoration. Edward IV returned in 1471 and defeated his opponents at Barnet and Tewkesbury. Henry's son was killed, and Henry died in the Tower soon afterward, almost certainly murdered, though responsibility and circumstances remain uncertain. His reign left enduring educational foundations alongside the collapse of English ambitions in France and a prolonged crisis of royal authority.