Born in London, Eccles first studied music under his father, Solomon Eccles. He was appointed to the King's band in 1694, and in 1700 became Master of the King's Musick. Also in 1700 he finished second in a competition to write music for William Congreve's masque The Judgement of Paris (John Weldon won).
Eccles was very active as a composer for the theatre, and from the 1680s wrote a large amount of incidental music including music for William Congreve's Love for Love, John Dryden's The Spanish Friar and William Shakespeare's Macbeth. Jointly with Henry Purcell he wrote incidental music for Thomas Durfey's Don Quixote. He became a composer to Drury Lane theatre in 1693 and when some of the actors broke off to form their own company at Lincoln's Inn Fields in 1695, he composed music for them as well. Eccles also wrote music for the coronation of Queen Anne and a number of songs.
For much of the later part of his life, Eccles lived in Kingston upon Thames and wrote little music apart from the occasional ode, instead spending much of his time fishing.
John Eccles is also the name of an Australian Nobel Prize winner.