Darnley was born in 1545, at Temple Newsam, Leeds, in the West Riding of Yorkshire, England. Through his parents he had claims to both the Scottish and English thrones, as he was descended from both James II of Scotland and Henry VII.  Darnley’s father, Matthew Earl of Lennox, had been declared guilty of treason in Scotland for his part in the war of the Rough Wooing, siding with the English as an opponent of Mary of Guise and Regent Arran, and his Scottish estates were forfeited in 1545. Lennox lived in exile in England for 22 years, returning to Scotland in 1564. Darnley’s mother, Margaret Douglas had left Scotland in 1528.  Lord Darnley was well educated and brought up conscious of his status and inheritance. He became well-versed in Latin and grew up familiar with Gàidhlig, English and French. He excelled in singing, lute playing, and dancing. His tutors included the Scottish scholar, John Elder, who had been an advocate of Anglo-Scottish union by the marriage of Mary, Queen of Scots, to Prince Edward, and gave his opinions to Henry VIII as the Advice of a Redshank in 1543. Another of his schoolmasters, Arthur Lallart, was interrogated in London after going to Scotland in 1562.  Darnley was strong and athletic, a good horseman with knowledge of weapons and a passion for hunting and hawking. Darnley wrote a letter to Mary I of England from Temple Newsam in March 1554 mentioning a drama or map he had made, the Utopia Nova. He wished, “every haire in my heade for to be a wourthy souldiour”.

The “Lennox crisis” was a political dilemma in England that arose from the dynastic ambition of the Lennoxes: Matthew Stewart, 4th Earl of Lennox, was third in line to the Scottish throne, and his wife Margaret Douglas was niece to Henry VIII and granddaughter of Henry VII.[7] The Lennox family were Roman Catholic and might therefore have represented an alternative succession in England.  When Henry II of France died in July 1559, Lennox’s brother, the Sieur d’Aubigny, was elevated in the French court as kinsman of the new queen, Mary, Queen of Scots. Aubigny arranged for Darnley to be dispatched to the French court to congratulate Mary and Francis II of France on their accession and seek restoration for Lennox. Mary did not restore Lennox to his Scottish earldom, but she did give 1,000 crowns to Darnley and invited him to her coronation. Lennox’s plan was to appeal directly to the Queen of Scots via her ambassador, above the heads of Elizabeth and the Guise. The mission of Lennox’s agent, one Nesbit, appears to have been a desperate one; not only was Lennox willing to hand over Darnley and his brother Charles as hostages for his restoration, but he supplied pedigrees of Darnley, indicating his right to the inheritance of England and Scotland and the houses of Hamilton and Douglas. Aubigny was also later accused of supporting Mary’s title to the throne of England and hinting that even his nephew had a stronger claim than Elizabeth.  Lennox set Nesbit to watch Mary, Darnley and Darnley’s tutor, John Elder. In 1559 Nicholas Throckmorton, the English ambassador in Paris, warned Elizabeth that Elder was “as dangerous for the matters of England as any he knew.”  The historian Sarah Macauley notes, “After the Queen of Scots, Lord Darnley was the strongest dynastic claimant to Elizabeth’s throne. He was also the natural choice for many of Elizabeth’s enemies as male, English-born and Catholic. Paget supposed in March 1560 that talk of the Catholics raising Darnley to the throne in the event of the Queen’s death was ‘well founded’.”

By the summer of that year, Elizabeth’s position was considerably strengthened. Francis Yaxley was one notable spy. A Catholic, Yaxley had been a clerk of the Signet and had been employed by William Cecil since 1549, travelling in France for him. Yaxley had placed Mabel Fortescue and other ladies as servants in the Lennox household at Settrington in November 1560. Yaxley had been employed by Margaret Douglas; his interrogation at the Tower of London in February 1562 revealed that he had obtained intelligence about the English Court from the Spanish ambassador, and the ambassador had entrusted him and Hugh Allen with messages and tokens for the Lennoxes and Darnley. Yaxley admitted that his missions were intended to arrange the marriage of the Queen of Scots with Darnley, that Darnley’s religion guaranteed him greater success in his suit than the Earl of Arran, and that Margaret Douglas had many friends “in the nurtht.” Although the Lennox threat never died out, Elizabeth did not convict the family of treason in 1562 after their arrest nor did she encourage steps made to annul Margaret’s claim to her throne by inquiring into her legitimacy. Perhaps, as has been suggested, Elizabeth feared that these investigations could also be directed at herself, or her inaction was intended merely to ensure the survival of the monarchy by not reducing the number of potential heirs. The Lennox family were released in February 1563, and within a few months, Darnley and his mother were conspicuous by their presence at Court and the favour they received there, although Elizabeth would not accommodate the Earl at Court.

On 3 February 1565 Darnley left London and by 12 February he was in Edinburgh. On 17 February he presented himself to Mary at Wemyss Castle in Fife. James Melville of Halhill reported that “Her Majesty took well with him, and said that he was the lustiest and best proportioned long man that she had seen.” After a brief visit to his father at Dunkeld, Darnley returned with Mary and the court to Holyrood on 24 February. The next day he heard John Knox preach, and he danced a galliard with Mary at night. From then on, he was constantly in Mary’s company.  Darnley was his wife’s first cousin through Margaret Tudor, putting both Mary and Darnley high in the line of succession for the English throne. Darnley was also a descendant of a daughter of James II of Scotland and so also in line for the throne of Scotland.  As a preliminary to the marriage, Darnley was made Lord of Ardmanoch and Earl of Ross at Stirling Castle on 15 May 1565. An entourage of 15 men were made knights, including one of Mary’s half brothers, Sir Robert Stewart of Strathdon, Robert Drummond of Carnock, and James Stewart of Doune Castle. In England, a concerned Privy council debated the perils of the intended marriage on 4 June 1565. One of their resolutions was to relax the displeasure shown to Lady Catherine Grey, another rival to Mary Stuart for the English throne. Mary sent John Hay, Commendator of Balmerino, to speak to Elizabeth; Elizabeth demanded Darnley’s return, and gave John Hay plainly to understand her small satisfaction.  On 22 July Darnley was made Duke of Albany in Holyrood Abbey and the banns of marriage were called in the parish of Canongate. A proclamation was made at the Cross of Edinburgh on 28 July that government would be in the joint names of the king and queen of Scots, thus giving Darnley equality with, and precedence over, Mary. This was confirmed in the circulation of a silver ryal in the names of Henry and Mary. On 29 July 1565 the marriage took place by Roman Catholic rites in Mary’s private chapel at Holyrood, but Darnley (whose religious beliefs were unfixed – he was raised as a Catholic, but was later was influenced by Protestantism) – refused to accompany Mary to the nuptial mass after the wedding itself.

Soon after Mary married Darnley, she became aware of his vain, arrogant and unreliable qualities, which threatened the well-being of the state. Henry was unpopular with the other nobles and had a violent streak, aggravated by his drinking. Mary refused to grant Darnley the Crown Matrimonial, which would have made him the successor to the throne if she died childless. By August 1565, less than a month after the marriage, William Cecil heard that Darnley’s insolence had driven Lennox from the Scottish court. Mary soon became pregnant.  Mary’s private secretary, David Rizzio was stabbed 56 times on 9 March 1566 by Lord Darnley and his friends in the presence of the seven-months-pregnant queen in her dining room. According to English diplomats Thomas Randolph and the Earl of Bedford, the murder of Rizzio (who was rumoured to be the father of Mary’s unborn child) was part of Darnley’s bid to force Mary to cede the Crown Matrimonial. Darnley also made a bargain with his allies to advance his claim to the Crown Matrimonial in the Parliament of Scotland in return for restoring their lands and titles.  When the Spanish Ambassador in Paris heard this news, the headlines were that Darnley “had murdered his wife, admitted the exiled heretics, and seized the kingdom.” However, on 20 March, Darnley posted a declaration denying all knowledge of or complicity in the Rizzio murder. Mary no longer trusted her husband and Darnley was disgraced by the kingdom. On 27 March, the Earl of Morton and Lord Ruthven, who were both present at Rizzio’s murder and had fled to England, wrote to Cecil claiming that Darnley had initiated the murder plot and recruited them, because of his “heich quarrel” and “deadly hatred” of Rizzio.

Mary and Darnley’s (or Rizzio’s) son James was born on 19 June 1566 at Edinburgh Castle. He was baptised Charles James on 17 December 1566 in a Catholic ceremony held at Stirling Castle. His godparents were Charles IX of France, Elizabeth I of England and Emmanuel Philibert, Duke of Savoy. Mary refused to let the Archbishop of St Andrews, whom she referred to as “a pocky priest”, spit in the child’s mouth, as was then the custom. In the entertainment, devised by Frenchman Bastian Pagez, men danced dressed as satyrs and sporting tails; the English guests took offence, thinking the satyrs “done against them”.  Following the birth of James the succession was more secure; in late 1566 and early 1567, Darnley and Mary appeared to be close to reconciliation as she was often seen visiting his chambers. Darnley, however, alienated many who would otherwise have been his supporters through his erratic behaviour. His insistence that he be awarded the Crown Matrimonial was still a source of marital frustration.

Darnley was murdered eight months after James’s birth. On 9 February 1567, his body and that of his valet were discovered in the orchard of Kirk o’ Field, in Edinburgh, where they had been staying.  During the weeks leading up to his death, Darnley was recovering from a bout of smallpox (or, it has been speculated, syphilis). He was described as having deformed pocks upon his face and body. He stayed with his family in Glasgow, until Mary brought him to recuperate at Old Provost’s lodging at Kirk o’ Field, a two-storey house within the church quadrangle, a short walk from Holyrood – with the intention of incorporating him into the court again.[29] Darnley stayed at Kirk o’ Field while Mary attended the wedding of Bastian Pagez, one of her closest servants, at Holyrood. Around 2 am on the night of 10 February 1567, while Mary was away, two explosions rocked the foundation of Kirk o’ Field. These explosions were later attributed to two barrels of gunpowder that had been placed in the small room under Darnley’s sleeping quarters. Darnley’s body and the body of his valet William Taylor, were found outside, surrounded by a cloak, a dagger, a chair and a coat. Darnley was dressed only in his nightshirt, suggesting he had fled in some haste from his bedchamber. Upon further examination, the bodies had no signs of injuries that could be associated with the explosion, so the blast was not considered to have killed Darnley. It was determined that the two men were killed by strangulation, believed to have taken place after the explosion.