Born about 1360, he was the younger son of John Cokayne (died 1372), of Ashbourne in Derbyshire, Chief Steward for the northern half of the Duchy of Lancaster, and his wife Cecily, daughter of Sir William Vernon, of Haddon and Harlaston, and his wife Margaret, daughter of Sir Robert Stopford.
His elder brother Edmund (died 1403) was heir to the family lands and John entered the law.
From 1398 to 1400 he followed his father as Chief Steward of the Duchy north of the Trent, an appointment by John of Gaunt who named Cokayne as one of the executors of his will.
[2] In 1425 he sat with the Chief Justice, Sir William Babington, on a case over parliamentary expenses brought by the borough of Bedford.
[5] The proceeds of his judicial offices allowed him to acquire country estates, first buying land at Bearwardcote in Derbyshire and then a life interest in manors at St Ippolyts and Radwell in Hertfordshire.