Sir John Montacute, the eldest son of Sir John Montacute by Margaret Monthermer, was born in or about the year 1350. His military career commenced when all the great victories of the Hundred Years War had already been achieved, and the English dominion in France was on the wane. He received knighthood, in 1369, from the Earl of Cambridge, in reward of his prowess at the Siege of Bourdeille, where two renowned captains, Ernaudon and Bernardet De Batefol, surrendered to him as prisoners. In the course of the same campaign, he was, with the rank of banneret, attached to the staff of that prince at Belle Perche, when the Duchess of Bourbon was carried from that fort in the view of her son's army. Upon those occasions, Froissart identifies him as nephew to the Earl of Salisbury, but where the name of "Sir John Montacute" occurs in the public records between the years 1370 and 1390 (the latter being the date of his father's death), it is difficult to decide whether it applies to father or son.

In 1391, our knight, having done homage for his patrimonial inheritance, obtained the King's license to journey into Prussia with a retinue of ten servants, probably in the same expedition against the Lithuanians in which the Earl of Derby (later Henry IV) bore a part. In the following year, he was summoned to Parliament as Lord Montagu and, in the Autumn of 1394, he attended King Richard II into Ireland. In the spring of 1395, he inherited the Monthermer estates, upon the decease of his mother, and, in 1396, was employed, for the last time, in a military capacity beyond sea.

The dignity and estates of John's uncle, William, Earl of Salisbury, devolved to him in 1397 and he was, about the same time, appointed a member of the Most Noble Order of the Garter. From that date, we find him constantly near the person of the King, whom he served with unabated attachment during the guilty and unhappy remnant of his reign. He naturally became, under such circumstances, one of the appellants against the monarch's opponents, Gloucester, Arundel and Warwick, and, upon the forfeiture of the last of those noblemen, eight of his escheated manors fell to his share.

Towards the close of 1398, Salisbury was nominated Marshal of England during the absence of the Duke of Surrey in Ireland and Froissart's narrative, that he was, about Christmas, entrusted with a negotiation of great delicacy at the French Court, seems to be corroborated by the record of a safe-conduct then granted to him. The design of his mission was to frustrate a proposed matrimonial alliance between the King's cousin, Henry, then Duke of Lancaster (later King Henry IV), and Mary, the daughter of the Duc de Berri; and Salisbury succeeded in that object. Upon his return, he was one of the peers who assented, in Parliament, to the repeal of the patent which had reserved to Henry the control over his estates during his exile. He was also joined in a commission, with others, to treat for a peace with Scotland, but it is doubtful whether he proceeded on that service, as he was certainly in the retinue of the King on his fatal expedition to Ireland in May 1399.

The intelligence of Lancaster's arrival in England induced Richard to despatch Salisbury from Ireland with a part of the English army to oppose him. Landing near Conway, the Earl was enabled to augment his forces by new levies in Wales and Cheshire, but the gentry of those districts, who had been persuaded to take up arms, dispersed upon finding the voyage of the King from Waterford protracted by adverse winds and hearing of the formidable approach of Henry after his successful visit to the metropolis. The unfortunate monarch, therefore, when he had at length reached the English coast, saw himself powerless and at the mercy of the invader.

Notwithstanding the hostile part which Salisbury and other loyal adherents of the fallen sovereign had taken against the usurper, it was the obvious policy of the latter to suppress his resentment. They were accordingly left unmolested during the first days of the new reign. But the throne had no sooner been secured to Henry by the unanimous consent of Parliament, than it was decided to wrest from Richard's late favourites the immense wealth which they had acquired by the confiscations of 1397. The appellants of that year were thus called upon for their justification. Salisbury, in his turn, endeavoured to extenuate his conduct upon grounds similar to those which had been pleaded by his former confederates, averring that he had not been the author or contriver of the bill of appeal, and his ignorance even of its purport until commanded by the late King to join in the proceeding. He had then only concurred, in common with his peers, in the judgments given thereon. Having also heard of the allegations of the Duke of Norfolk that he had compassed the death of the late Duke of Lancaster, Salisbury declared he was ready, if Norfolk were present, or if any other person should repeat such false assertions, to defend himself, as a gentleman in any way the new King might think fit. For the rest, he repented of his error and threw himself upon the mercy of God, the King and his crown. The Duke of Norfolk was then no more; but the Lord Morley appears to have risen to repeat the accusation against Salisbury and the latter to have defied him to prove it by wager of battle. The duel between these noblemen was appointed to be held at Newcastle-on-Tyne, probably on the King's expedition by Scotland; but there seems to be little evidence that the meeting took place.

It is remarkable that Salisbury should have been excepted from the parliamentary sentence by which his associates in the appeal were deprived of the grants of land made to them subsequent to the ruin of Gloucester and his party. For John hastily and treacherously requited King Henry's forbearance towards him. At the close of the parliamentary session, he conspired, with Albemarle, Exeter and Surrey (then degraded to their former titles of Rutland, Huntingdon and Kent), to seize and destroy the King. However, having travelled to a joust in Windsor for that purpose, they failed in their objective and Salisbury accompanied the Earl of Kent in open rebellion into the western counties. Having been (according to the narrative generally received by historians, and confirmed by the allegations of a petition presented by his son in the following reign) overpowered and detained in custody at Cirencester (Glos), for a day and a half, with promise that he should be safely delivered up to the King, Salisbury was, in consequence of some sudden attempt to rescue him, beheaded by the townsmen on the 7th January 1400.

Most of his remains were deposited in Cirencester Abbey, while his head is said to have been sent to London. However, upon the petition of his widow, to King Henry V in 1420, they were permitted to be removed to Bisham Priory in Berkshire, the foundation of his ancestor adjoining the family home.

Walsingharn relates, with acrimony, that the Earl had been a chief patron of the sect of Wycliffe, known as the Lollards, having carried his iconoclastic zeal so far as to destroy all the images of saints which had been set up in his Chapel at Shenley (Herts) by Aubrey and Buxhull, his wife's former husbands, excepting that of St. Catherine, which, being an object of particular veneration to his household, he allowed to remain in his bake-house. The chronicler adds, that he became contrite just before his execution and expressed an ardent desire to be shriven according to the rites of the mother church.