Poynter was born in Paris to an architect father and a mother who was grand-daughter of the sculptor Thomas Banks. He decided to become a painter on meeting Frederic Leighton in Rome in 1854, and Leighton remained his life-long mentor and hero. The works of the two men epitomize Victorian neo-classicism and the inspiration for Poynter's frieze-like compositions and fluttering drapery is clear. Technically accomplished, he was also concerned with the accuracy of archaeological detail. This precision, alongside an innate understanding of the nude, was indicative of his championing of the Academic tradition.
He began to exhibit at the Royal Academy in 1861 (the present example being shown in 1917, two years prior to his death) and five years later married Burne Jones's sister-in-law Agnes MacDonald. Whilst already respected by his peers, his career accelerated on a more public level as he embarked on a teaching career in 1871 running the newly-founded Slade School of Art. This was followed by an interlude as principal of the National Art Training School before he accepted the directorship of the National Gallery. He held the post until 1904, combining it for eight years with that of President of the Royal Academy (he succeeded Millais in 1896). Poynter is the only artist ever to have occupied the two positions concurrently, while in remaining P.R.A. until 1918, he enjoyed one of the longest tenures of any incumbent. He was knighted in 1896 and created a baronet in 1902. This distinguished career, marked with countless honours, earned him a burial in St. Paul's Cathedral.