[1] Having taken holy orders in 1560, he became chaplain to Richard Cox, Bishop of Ely, who collated (that is, appointed) him to the rectory of Teversham, just to the east of Cambridge.

In 1563 he was appointed Lady Margaret's Professor of Divinity at the University of Cambridge, and his lectures gave such satisfaction to the authorities that on 5 July 1566 they considerably augmented his stipend.

He had a principal share in compiling the statutes of the university, which passed the great seal on 25 September 1570, and in the November following he was chosen as vice-chancellor.

Puritan satirists would later mock Whitgift as "Perne's boy" who was willing to carry his cloak-bag – thus suggesting that the two had enjoyed a homosexual relationship.

[3] As their tutor, Whitgift bought the brothers their early classical text books, including works by Plato, Cicero and others.

Thomas Macaulay's description of Whitgift as "a narrow, mean, tyrannical priest, who gained power by servility and adulation..." is, according to the author of his 1911 Encyclopædia Britannica entry, "tinged with rhetorical exaggeration; but undoubtedly Whitgift's extreme High Church notions led him to treat the Puritans with exceptional intolerance".

On 24 March 1577, Whitgift was appointed Bishop of Worcester, and during the absence of Sir Henry Sidney in Ireland in 1577 he acted as vice-president of Wales.

In August 1583 he was appointed Archbishop of Canterbury to replace Edmund Grindal, who had been placed under house arrest after his disagreement with Queen Elizabeth over "prophesyings" and died in office.

Whitgift had nine leading presbyterians including Thomas Cartwright arrested in 1589–90, and though their trial in the Star Chamber for sedition did not result in convictions they did agree to abandon their movement in return for freedom.

[7] Whitgift took a strong line against the Brownist movement and their Underground Church in London led by Henry Barrow and John Greenwood.

"[8] Whitgift was the prime mover behind the Act against Seditious Sectaries which was passed in 1593, making Separatist Puritanism a felony, and he had Barrow and Greenwood executed the following morning.

Whitgift is described by his biographer, Sir George Paule, as of "middle stature, strong and well shaped, of a grave countenance and brown complexion, black hair and eyes, his beard neither long nor thick."

His Collected Works, edited for the Parker Society by John Ayre (3 vols., Cambridge, 1851–1853), include the controversial tracts mentioned above, two sermons published during his lifetime, a selection from his letters to Cecil and others, and some portions of his previously unpublished manuscripts.