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While in the care of her brother-in-law Jasper Tudor, on 28 January 1457, the Countess gave birth to a son, Henry Tudor, at Pembroke Castle. She was thirteen years old at the time and not yet physically mature, so the birth was extremely difficult. In a sermon delivered after her death, Margaret’s confessor, John Fisher, deemed it a miracle that a baby could be born “of so little a personage”. Her son’s birth may have done permanent physical injury to Margaret; despite two later marriages, she never had another child. Years later, she enumerated a set of proper procedures concerning the delivery of potential heirs, perhaps informed by the difficulty of her own experience.

Shortly after her re-entry into society after the birth, Jasper helped arrange another marriage for her to ensure her son’s security. She married Sir Henry Stafford (c. 1425–1471), the second son of Humphrey Stafford, 1st Duke of Buckingham, on 3 January 1458, at the age of fourteen. A dispensation for the marriage was necessary because Margaret and Stafford were second cousins; it was granted on 6 April 1457.

They enjoyed a fairly long and harmonious marital relationship and were given Woking Palace, to which Margaret sometimes retreated and which she restored. Margaret and her husband were given 400 marks’ worth of land by Buckingham, but her own estates were still their main source of income. For a time the Staffords were able to visit Margaret’s son, who had been entrusted to Jasper Tudor’s care at Pembroke Castle in Wales.

Years of York forces fighting Lancastrian for power culminated in the Battle of Towton in 1461, where the Yorkists were victorious. Edward IV was King of England. The fighting had taken the life of Margaret’s father-in-law and forced Jasper Tudor to flee to Scotland and France to muster support for the Lancastrian cause. Edward IV gave the lands belonging to Margaret’s son to his own brother, the Duke of Clarence. Henry became the ward of Sir William Herbert. Again, Beaufort was allowed some visits to her son.

In 1469 the discontented Duke of Clarence and Earl of Warwick incited a rebellion against Edward IV, capturing him after a defeat of his forces. Beaufort used this opportunity to attempt to negotiate with Clarence, hoping to regain custody of her son and his holdings. Soon, however, Edward was back in power.

Warwick’s continued insurrection resulted in the brief reinstallation of the Lancastrian Henry VI in 1470–71, which was effectively ended with the Yorkist victory at the Battle of Barnet. Faced with York rule once again, Margaret allegedly begged Jasper Tudor, forced to flee abroad once more, to take thirteen-year-old Henry with him. It would be fourteen years before Beaufort saw her son again.

In 1471, Margaret’s husband, Lord Stafford, died of wounds suffered at the Battle of Barnet, fighting for the Yorkists. At 28 years old, Margaret became a widow again.

The Countess always respected the name and memory of Edmund as the father of her only child. In 1472, sixteen years after his death, Margaret specified in her will that she wanted to be buried alongside Edmund, even though she had enjoyed a long, stable and close relationship with her third husband.

In June 1472, Margaret married Thomas Stanley, the Lord High Constable and King of the Isle of Mann.

Their marriage was primarily one of convenience; marrying Stanley enabled Margaret to return to the court of Edward IV and Elizabeth Woodville. Indeed, Gristwood speculates Beaufort organized the marriage with the sole aim of rehabilitating her image and securing herself a prime position from which to advocate for her son. Evidently her efforts were successful; Margaret was chosen by Queen Elizabeth to be godmother to one of her daughters.

Holinshed, a Tudor chronicler, claims King Edward IV later proposed a marriage between Beaufort’s son and his own daughter, Elizabeth of York, intending to force Henry Tudor out of his safe haven on the continent.

Poet Bernard Andre seems to corroborate this, writing of Tudor’s miraculous escape from the clutches of Edward’s envoys, allegedly warned of the deception by none other than his mother.