Although Henry was officially king of France, he never had much opportunity to rule it. In France Charles VI's nineteen-year-old son was also declared king as Charles VII. He held most of the southern provinces while Henry's regent, his uncle, John, duke of Bedford, governed the northern provinces for England. The battle for France dragged on, lacking the relentless drive and power of Henry V. Bedford endeavoured to consolidate the gains the English had made so that the benefits could be ploughed back to the crown and thus reduce the drain of the war on the English treasury. However this meant that any final victory was perpetually deferred. Neither Bedford nor the rather weak-willed Charles VII had sufficient skill to conclude the battle. The key to the fighting centred around Orleans which came under siege in 1427. This was the period of Joan of Arc who galvanised the French into action. Although she was only seventeen she led an army into Orleans and raised the siege in May 1429. The spirit of victory was restored to the French and a wave of national pride engulfed the country as they regained lands from the English along the Loire Valley. Charles was crowned king of France in June 1429. This concerned Bedford who urged on the coronation of young Henry. He was crowned king of England in November 1429, but it was another two years before he was crowned as king of France in 1431. He was the only king ever to be formally crowned in both countries. However, although it had been hoped this would instil a similar nationalistic fervour in the English, it achieved nothing. The French were gaining the upper hand and the English were losing all of the lands Henry V had gained. In 1435 the Duke of Burgundy, in whose name the English had first invaded France, reached an agreement with Charles VII known as the Treaty of Arras. From then on the English cause in France was lost; Charles entered Paris in 1436. Apparently when Henry learned of Burgundy's defection he cried. Although he retained the title of king of France, it held no authority. The conflict would continue for another eighteen years until the death of England's dashing champion John Talbot, earl of Shrewsbury, at Castillon in 1453. With that defeat England's Hundred Years' War with France came to an end. The only French territory remaining in English hands was Calais.

Henry did not declare himself of age until November 1437, just before his sixteenth birthday. Until then the protector of England had been his uncle, Humphrey, duke of Gloucester. No one seemed to like Gloucester, and he was not trusted with full regency powers, which had remained with Bedford until his death in 1435. The result was constant wrangles in Parliament as Gloucester endeavoured to exercise his authority. At times even the young king interceded to calm matters, although no one took much notice of young Henry. During his upbringing he had been told to behave himself and not believe himself to have absolute authority. By the time he took the reins of government he was already a pawn of the most powerful statesmen and was too weak willed to exert any power. This was not because he did not believe he should, it was mostly because he was not interested. People are not simply born kings, they have to be them, and Henry had no will to govern. As a result he invested power and authority in the hands of those he most trusted and, as Henry was amazingly naive, these tended to be the least scrupulous of people. Amongst them was William de la Pole, earl of Suffolk, and grandson of Michael de la Pole who had been one of RICHARD II’s court favourites. Although de la Pole ingratiated himself into Henry's affections, and became his steward in 1435, he had good intentions since he was a peacemaker at heart. However, his solution for peace effectively meant the loss of France, and his chief opponent in this was Humphrey of Gloucester who was in favour of continuing the war of conquest. In other times, history might have been on the side of Suffolk, but in the years so soon after Henry V's great victories and with so many lives and resources expended, the English nation was not for sacrificing France. Nevertheless, because of his closeness to the king, Suffolk was able to plot his course for some years. It was through Suffolk's negotiations that Henry married Margaret of Anjou in 1444 with terms that should have brought peace. What many did not know until later was that one of the terms in order to extend the truce was that Henry would surrender Maine, to which he agreed. There was uproar when the truth was known to the extent that Henry no longer felt safe in London. Margaret of Anjou together with the Earl of Suffolk convinced Henry that his uncle was plotting an uprising. Humphrey of Gloucester was arrested and confined at Bury St Edmunds in February 1447, where he died a week later. Many believed that he was murdered, probably on Suffolk's orders. Suffolk, realising his unpopularity, switched from peacemaker to warmonger and invaded Brittany in 1449. This brought the conflict into Normandy, which the French conquered by September 1450. Suffolk could not escape the loss of Normandy. Even before the war was concluded, Suffolk was arrested and impeached. Henry, hoping to save his life, had him banished, but his ship was intercepted at Dover and Suffolk was executed. Suffolk and his allies now became the scapegoat for all that had gone wrong both in France and with the mismanagement of English affairs. This was the main cause for the revolution led by John Cade in May 1450 which followed much the same course as the Peasants' Revolt of seventy years earlier, except that Henry VI did not show the bravery of the young Richard 11. The revolt ran its course over the next two months before Cade's death. His rebellion was an opportunity to purge government, but Henry took little action. Instead he created further polarisation by appointing Edmund Beaufort, the Duke of Somerset (and Henry V's first cousin), as his closest adviser. Somerset had once been a good soldier, but his role as lieutenant of France had coincided with the loss of most of the English lands, and he was regarded as the focal point for English failure. He was also the sworn enemy of Richard, duke of York (who was Henry V's second cousin). York had been effectively banished to Ireland in 1447, because of his sympathy for Humphrey of Gloucester. However in August 1450 he returned to England, supported by his army, and demanded his place on the Council. The next few years were tense ones as the rivalry between Somerset and York grew: a rivalry that would erupt into the Wars of the Roses. Somerset had the upper hand to begin with, because of his direct link with the king, but matters changed after August 1453 when the king became afflicted by the first bouts of mental decline that would darken his later years. This was almost certainly inherited from his grandfather, the king of France, who also had bouts of imbecility. Exactly what was wrong with Henry is not certain, but he lost all memory and reason and would sit for weeks devoid of expression or awareness in a deep melancholia. The depression may have been triggered by the loss of France. It came just two months before the birth of Henry's first (and only) son, Edward. The king gave no sign of acknowledging the child and when, eighteen months later, Henry's reason returned, he had no idea where the child came from, believing it must have been born of the Holy Ghost.

Richard of York was made "Protector of the Realm" in March 1454 and promptly had Somerset arrested and imprisoned in the Tower. However, a year later, when Henry recovered, the king had Somerset released and York dismissed. York's entreaties to the king were ignored and the inevitable conflict broke out at St Albans on 22 May 1455. The battle was brief and Somerset was killed. That should have been an end of any hostilities, because Henry seemed prepared to be reconciled to Richard of York. When another bout of madness struck Henry in November 1455, Richard was again made protector but was again dismissed in February 1456. With Henry scarcely able to govern, his queen, Margaret, took up his cause. She despised the arrogant haughtiness of York and encouraged the new duke of Somerset, Henry Beaufort, against him. By 1458 the flames of war were being fanned across England between the Yorkists, supported by Richard Neville, earl of Salisbury, and his son, also Richard Neville, earl of Warwick, on the one side, and the Lancastrians, under the figurehead of Henry VI, but really led by Margaret of Anjou, supported by Somerset and Henry Percy, the third earl of Northumberland. With the battle of Ludlow in 1459 the Wars of the Roses began in earnest. At that battle the Yorkists were routed and Richard of York fled to Wales and then Ireland, while his supporters sought refuge in Calais. The following year the Calais element defeated the Lancastrians at Northampton, and Richard of York returned to England. He now formally placed his claim to the throne before Parliament in September 1460. The following month his right was acknowledged and he was declared the heir to the throne, in place of Henry's son Edward. Henry, his mind failing rapidly, agreed, but Margaret of Anjou was not so easily pacified. She raised a further army in the north and met the Yorkists at Wakefield on 30 December. York was killed in the battle, whilst Salisbury was captured and murdered. Margaret marched on London, defeating the earl of Warwick at St Albans early in 1461. Warwick managed to recruit another army, together with York's son, Edward, and they marched into London in triumph in March 1461. Edward declared himself king (as Edward IV). His forces marched north, following the retreating army of Henry and Margaret, and the two clashed at Towton near Tadcaster in Yorkshire. There, in the middle of a snowstorm, the Lancastrian army was defeated. Henry and Margaret fled to Scotland, where they were given refuge by the young king James III. Henry bought support from the Scots by granting them Berwick, but the military aid he was given proved useless in the abortive battle at Carlisle. Edward was soon after crowned king of England. He outsmarted every move made by Margaret of Anjou, including her alliance with France, to try and regain the crown and, after three years, Henry became an embarrassment to the Scots. He was smuggled out of Scotland and spent a year in refuge in northern England, until he was betrayed and captured by English forces in July 1465 and imprisoned in the Tower of London.

Had Henry been of the same arrogant disposition Of Edward II and Richard II, both of whom had been murdered in prison, Henry might have expected his days to be numbered. But following an amazing reversal in the fortunes of Edward IV, Henry suddenly found himself removed from the Tower on 3 October 1470 and reinstated as king. The earl of Warwick had changed his allegiance to Henry and even went so far, two months later, as to marry his daughter Anne to the king's son, Edward. Henry's 'readeption', as it was known, was not to last for long. Edward IV returned with an army in April and defeated and killed Warwick. The king was again captured and imprisoned. His wife's army arrived too late to save him. She and her supporters were defeated at Tewkesbury on 4 May 1471, where the young Prince Edward was killed. Margaret was also imprisoned in the Tower and on that same night, 21 May, Henry was stabbed to death. Just who killed him was never revealed, though his body was displayed in its coffin the next day as if he had died naturally, so as to avoid any later rebellion to restore him.

Margaret of Anjou remained in prison, first at the Tower, then Windsor and finally Wallingford, before being released to return to her father's estates at Angers in 1475. Her appearance had become as wretched as Henry's, exhausted by years of trial and tribulation. Had she been the queen of a stronger king, they would have made a remarkable pair and doubtless ruled with considerable effect, but Margaret had the misfortune to be married to a king who began weak and sank into mental decline. He should have been a younger brother and left government to John, duke of Bedford, who was much more able. Henry was more a scholar than a statesman. Although his reign led to the Wars of the Roses, he and his queen may best be remembered as the founders of King's College (1441) and Queen's College (1448) at Cambridge.