After the Restoration, as Dryden quickly established himself as the leading poet and literary critic of his day, he transferred his allegiances to the new government. Along with Astraea Redux, Dryden welcomed the new regime with two more panegyrics: To His Sacred Majesty: A Panegyric on his Coronation (1662) and To My Lord Chancellor (1662). These poems suggest that Dryden was looking to court a possible patron, but he was to instead make a living in writing for publishers, not for the aristocracy, and thus ultimately for the reading public. These, and his other nondramatic poems, are occasional—that is, they celebrate public events. Thus they are written for the nation rather than the self, and the Poet Laureate (as he would later become) is obliged to write a certain number of these per annum. In November 1662 Dryden was proposed for membership in the Royal Society, and he was elected an early fellow. However, Dryden was inactive in Society affairs and in 1666 was expelled for non-payment of his dues.
On 1 December 1663 Dryden married the royalist sister of Sir Robert Howard—Lady Elizabeth. Dryden's works occasionally contain outbursts against the married state but also celebrations of the same. Thus, little is known of the intimate side of his marriage. Lady Elizabeth bore three sons and outlived her husband.
With the reopening of the theatres after the Puritan ban, Dryden wrote plays. His first play, The Wild Gallant, appeared in 1663 and was not successful but was still promising, and from 1668 on he was contracted to produce three plays a year for the King's Company in which he became a shareholder. During the 1660s and '70s, theatrical writing was his main source of income. He led the way in Restoration comedy, his best-known work being Marriage à la Mode (1672), as well as heroic tragedy and regular tragedy, in which his greatest success was All for Love (1678). Dryden was never satisfied with his theatrical writings and frequently suggested that his talents were wasted on unworthy audiences. He thus was making a bid for poetic fame off-stage. In 1667, around the same time his dramatic career began, he published Annus Mirabilis, a lengthy historical poem which described the English defeat of the Dutch naval fleet and the Great Fire of London in 1666. It was a modern epic in pentameter quatrains that established him as the preeminent poet of his generation, and was crucial in his attaining the posts of Poet Laureate (1668) and historiographer royal (1670).
When the Great Plague of London closed the theatres in 1665 Dryden retreated to Wiltshire where he wrote Of Dramatick Poesie (1668), arguably the best of his unsystematic prefaces and essays. Dryden constantly defended his own literary practice, and Of Dramatick Poesie, the longest of his critical works, takes the form of a dialogue in which four characters–each based on a prominent contemporary, with Dryden himself as 'Neander'—debate the merits of classical, French and English drama. The greater part of his critical works introduce problems which he is eager to discuss, and show the work of a writer of independent mind who feels strongly about his own ideas, ideas which demonstrate the breadth of his reading. He felt strongly about the relation of the poet to tradition and the creative process, and his best heroic play Aureng-zebe (1675) has a prologue which denounces the use of rhyme in serious drama. His play All for Love (1678) was written in blank verse, and was to immediately follow Aureng-Zebe. On 18 December 1679 he was attacked in Rose Alley near his home in Covent Garden by thugs hired by John Wilmot, 2nd Earl of Rochester, with whom he had a long-standing conflict.
Dryden's greatest achievements were in satiric verse: the mock-heroic Mac Flecknoe, a more personal product of his Laureate years, was a lampoon circulated in manuscript and an attack on the playwright Thomas Shadwell. Dryden's main goal in the work is to "satirize Shadwell, ostensibly for his offenses against literature but more immediately we may suppose for his habitual badgering of him on the stage and in print." It is not a belittling form of satire, but rather one which makes his object great in ways which are unexpected, transferring the ridiculous into poetry. This line of satire continued with Absalom and Achitophel (1681) and The Medal (1682). His other major works from this period are the religious poems Religio Laici (1682), written from the position of a member of the Church of England; his 1683 edition of Plutarch's Lives Translated From the Greek by Several Hands in which he introduced the word biography to English readers; and The Hind and the Panther, (1687) which celebrates his conversion to Roman Catholicism.
He wrote Britannia Rediviva celebrating the birth of a son and heir to the Catholic King and Queen on 10 June 1688. When later in the same year James II was deposed in the Glorious Revolution, Dryden's refusal to take the oaths of allegiance to the new monarchs, William and Mary, left him out of favour at court. Thomas Shadwell succeeded him as Poet Laureate, and he was forced to give up his public offices and live by the proceeds of his pen. Dryden translated works by Horace, Juvenal, Ovid, Lucretius, and Theocritus, a task which he found far more satisfying than writing for the stage. In 1694 he began work on what would be his most ambitious and defining work as translator, The Works of Virgil (1697), which was published by subscription. The publication of the translation of Virgil was a national event and brought Dryden the sum of £1,400. His final translations appeared in the volume Fables Ancient and Modern (1700), a series of episodes from Homer, Ovid, and Boccaccio, as well as modernised adaptations from Geoffrey Chaucer interspersed with Dryden's own poems. As a translator, he made great literary works in the older languages available to readers of English.
Dryden died on 12 May 1700, and was initially buried in St. Anne's cemetery in Soho, before being exhumed and reburied in Westminster Abbey ten days later. He was the subject of poetic eulogies, such as Luctus Brittannici: or the Tears of the British Muses; for the Death of John Dryden, Esq. (London, 1700), and The Nine Muses.
A Royal Society of Arts blue plaque commemorates Dryden at 43 Gerrard Street in London's Chinatown.