He was descended from Richard Talbot, a tenant in 1086 of Walter Giffard at Woburn and Battlesden in Bedfordshire. The Talbot family were vassals of the Giffards in Normandy. Hugh Talbot, probably Richard's son, made a grant to Beaubec Abbey, confirmed by his son Richard Talbot in 1153. This Richard (died 1175) is listed in 1166 as holding three fees of the Honour of Giffard in Buckinghamshire. He also held a fee at Linton in Herefordshire, for which his son Gilbert Talbot (died 1231) obtained a fresh charter in 1190. Gilbert's grandson Gilbert (died 1274) married Gwenlynn Mechyll, daughter and sole heiress of the Welsh Prince Rhys Mechyll, whose armorials the Talbots thenceforth assumed in lieu of their own former arms. Their son Sir Richard Talbot, who signed the Barons' Letter of 1301, held the manor of Eccleswall in Herefordshire in right of his wife Sarah, sister of William de Beauchamp, 9th Earl of Warwick. In 1331 Richard's son Gilbert Talbot (1276–1346) was summoned to Parliament, which is considered evidence of his baronial status – see Baron Talbot. Gilbert's son Richard married Elizabeth Comyn, bringing with her the inheritance of Goodrich Castle.
John Talbot was born in about 1384 or more likely around 1387 as second son of
Richard Talbot (4th Baron Talbot) of Goodrich Castle by
Ankaret, daughter and sole heiress of the
4th Baron Strange of Blackmere. His birthplace was Black Mere Castle (the caput of his mother's estates) near Whitchurch, Shropshire, which is now a scheduled monument listed as Blakemere Moat, site of the demolished fortified manor house. His younger brother Richard became Archbishop of Dublin and Lord Chancellor of Ireland: he was one of the most influential Irish statesmen of his time, and his brother's most loyal supporter during his often troubled years in Ireland. John also had an elder brother, Gilbert (born 1383), who was heir to their parents' baronies of Talbot and Strange.
His father died in 1396 when Talbot was just nine years old, and so it was Ankaret's second husband,
Thomas Neville, Lord Furnivall, who became the major influence in his early life. The marriage (1401) also gave the opportunity of a title for her second son, as Neville had no sons, with the title Baron Furnivall going through his eldest daughter Maud (Talbot's stepsister), who would become John's first wife. Their marriage resulted in John styling himself as John Talbot, 6th Baron Furnivall.