John de la Pole was born on 27 September 1442, only son and heir to William de la Pole, 1st Duke of Suffolk, and Alice Chaucer, the granddaughter of the poet Geoffrey Chaucer. John was therefore still only a child of seven when, on 7 February 1450, he was married to the six-year-old Lady Margaret Beaufort, though the Papal dispensation to marry was not signed until 18 August 1450.
The earldom of Suffolk, says historian Michael Hicks, was 'not particularly well-endowed,' probably only just scraping the £666 qualifying income for that rank. His mother, though, held substantial estates in her own right, from her father, Sir Thomas Chaucer. Furthermore, because this was Alice's third marriage, she held large dowers from both previous husbands, the second of whom had been Thomas Montagu, 4th Earl of Salisbury.
Arms of De la Pole: Azure, a fess between three leopard's faces or
John's father augmented the family's position by exploiting the favour of the King, Henry VI, to whom he was an important councillor in the 1440s. Already Earl of Suffolk, John's father was in turn elevated to a marquess (in 1444) and then Duke of Suffolk (1448), and with these titles received major grants from the crown. Also, it had been his father's receipt of the wardship of Margaret Beaufort from the king that enabled John's marriage to her, whilst both were still infants and despite them being within the prohibited degrees of consanguinity. Contemporaries claimed that the marriage to the daughter of John Beaufort, Duke of Somerset (cousin of the-then childless king) was intended to make John de la Pole an eventual heir to the crown; this is considered unlikely by modern historians, who have pointed at indications that the King supported William in these plans. It has been suggested that the marriage was the direct result of William's political difficulties during the 1450-1 parliament.
Any plans his father had for John were rudely upset in 1450 when Suffolk was impeached by parliament over the loss of Normandy in the Hundred Years' War. Suffolk was exiled, but never reached the continent as he was murdered by sailors in the Channel soon after his departure. On 30 April 1450, before he sailed from Ipswich, the disgraced duke wrote a letter to John in which he urged his son to "...flee the company and council of proude men, of coveitows men and of fateryng men...".
Since Suffolk had never been formally convicted, he was not attainted, but the royal grants which had given John de la Pole such good prospects were now resumed to the crown. And although John inherited his father's dukedom of Suffolk, he had lost the various offices that he had held, such as the Constableship of Wallingford Castle. On top of this, due to his mother retaining one-third of his father's estate in dower, his expectations from the dukedom could only have been even smaller. His income has been estimated at less than £280 per annum, which was less than the minimum required for an earl, let alone a duke.
John de la Pole did not come of age until 1463. As such, in 1450 his wardship was resumed to the crown, and custody of his estates granted to others by the king. His marriage to Margaret Beaufort was annulled, in February 1453. A recent biographer of her son (the later King Henry VII) has described them as being married "only nominally", and elsewhere as a "hasty measure destined not to last".