The Beaufort children were declared legitimate twice by parliament during the reign of King Richard II of England, in 1390 and 1397, as well as by Pope Boniface IX in September 1396. Even though they were the grandchildren of Edward III and next in the line of succession after their father's legitimate children by his first two wives, the Beauforts were barred from succession to the throne by their half-brother Henry IV.
John was created Earl of Somerset on 10 February 1397, just a few days after the legitimation of the Beaufort children was recognized by Parliament. The same month, he was also appointed Admiral of the Irish fleet, as well as Constable of Dover Castle and Warden of the Cinque Ports. In May, his admiralty was extended to include the northern fleet. That summer, the new earl became one of the noblemen who helped Richard II free himself from the power of the Lords Appellant. As a reward, he was created Marquess of Somerset and Marquess of Dorset on 29 September, and sometime later that year he was made a Knight of the Garter and appointed Lieutenant of Aquitaine. In addition, two days before his elevation as a Marquess he married the king's niece, Margaret Holland, sister of Thomas Holland, 1st Duke of Surrey, another of the counter-appellants. John remained in the king's favour even after his older half-brother Henry Bolingbroke (later Henry IV) was banished from England in 1398.
After Richard II was deposed by Henry Bolingbroke in 1399, the new king rescinded the titles that had been given to the counter-appellants, and thus John Beaufort became merely Earl of Somerset again. Nevertheless, he proved loyal to his half-brother's reign, serving in various military commands and on some important diplomatic missions. It was Beaufort who was given the confiscated estates of the Welsh rebel leader Owain Glyndŵr in 1400, although he would not have been able to take possession of these estates unless he had lived until after 1415. In 1404, he was named Constable of England.
John Beaufort and his wife Margaret Holland, the daughter of Thomas Holland, 2nd Earl of Kent and Alice FitzAlan, had six children. His granddaughter Lady Margaret Beaufort married Edmund Tudor, 1st Earl of Richmond, the son of Dowager Queen Catherine of Valois by Owen Tudor.