John Locke's Two Treatises of Government is by far the most celebrated work among those of Filmer's three major Whig critics and is generally recognized as a classic of early modern thought. Although it was written more or less contemporaneously with Tyrrell's Patriarcha, Non Monarcha and Sidney's Discourses Concerning Government, the fame and influence of the Two Treatises as one of the seminal texts of liberal thought has far outlasted those of these other Whig works. But before he was a philosophical legend, Locke was a relatively unknown partisan Whig. John Locke was born in 1632 into a West Country gentry family with small but prosperous estates in Somerset near Bristol. In contrast to his friend James Tyrrell, Locke's family loyalties were decidedly parliamentarian in the civil war, with his father, a successful attorney, serving as a captain in a parliamentary regiment of horse commanded by a local notable, Alexander Popham. Popham was elected to the Long Parliament in 1646, the same year as Algernon Sidney, and it was through Popham's patronage that Locke was admitted to the prestigious Westminster School that same year. In 1652 he entered Christ Church, Oxford, graduating with an M.A. in 1658, the same year Tyrrell began his matriculation.

Locke thus began a long but often troubled relation with Oxford University that would span over three decades. In his student days Locke acquired a keen interest in science and philosophy and shed much of the dogmatism of his Puritan background.