His father was killed in 1455 at the First Battle of St Albans.When his eldest brother, Henry Beaufort, 3rd Duke of Somerset, was killed fighting for Lancaster in 1464 at the Battle of Hexham, the next brother, Edmund, succeeded to the Dukedom, and John became "Marquess of Dorset" and "Earl of Dorset", courtesy titles granted to the Beaufort heir-apparent or heir-presumptive.
These titles were not recognized by King Edward IV, of the House of York.
When Henry VI of Lancaster reclaimed the throne in October 1470, John returned with his brother Edmund.
John was killed in the Battle of Tewkesbury on 4 May 1471, while fighting beside Edmund, who was captured and beheaded two days later.
With the death of John and Edmund, the legitimate male line of the Beauforts ended.