Collier was from a talented and successful family. His grandfather, John Collier, was a Quaker merchant who became a Member of Parliament. His father (who was a Member of Parliament, Attorney General and, for many years, a full-time judge of the Privy Council) was created the first Lord Monkswell. He was also a member of the Royal Society of British Artists. John Collier's elder brother, the second Lord Monkswell, was Under-Secretary of State for War and Chairman of the London County Council. In due course, Collier became an integral part of the family of Thomas Henry Huxley PC, sometime President of the Royal Society. Collier married two of Huxley's daughters and was "on terms of intimate friendship" with his son, the writer Leonard Huxley.
Collier's first wife, in 1879, was Marian (Mady) Huxley. She was a painter who studied, like her husband, at the Slade and exhibited at the Royal Academy and elsewhere. After the birth of their only child, a daughter, she suffered severe post-natal depression and was taken to Paris for treatment where, however, she contracted pneumonia and died in 1887.
In 1889 Collier married Mady's younger sister Ethel Huxley. Until the Deceased Wife's Sister's Marriage Act 1907 such a marriage was not possible in England, so the ceremony took place in Norway. Collier's daughter by his first marriage, Joyce, was a portrait miniaturist, and a member of the Royal Society of Miniature Painters. By his second wife he had a daughter and a son, Sir Laurence Collier KCMG, who was the British Ambassador to Norway 1941-51.
Collier's range of portrait subjects was broad. His commissioned portrait of the future King George V as Master of Trinity House in 1901 when Duke of York, and the Duke of Windsor when Prince of Wales were his major royal portraits. Other subjects included two Lord Chancellors, The Speaker of the House of Commons, Rudyard Kipling, Sir Lawrence Alma-Tadema, two Indian maharajahs, and Charles Darwin. A photocopy of John Collier's Sitters Book (made in 1962 from the original in the possession of the artist's son) can be consulted in the National Portrait Gallery Heinz Archive and Library. This is the artist's own handwritten record of all his portraits, including name of subject, date, fee charged, and details of any major exhibitions of the picture in question.
Collier died in 1934. His entry in the Dictionary of National Biography compares his work to that of Frank Holl because of its solemnity. This is only true, however, of his many portraits of distinguished old men — his portraits of younger men, women and children, and his so-called "problem pictures", covering scenes of ordinary life, are often very bright and fresh. The Dictionary of Portrait Painters in Britain describes his portraits as "painterly works with a fresh use of light and colour".
Sixteen of John Collier's paintings are now in the collections of the National Portrait Gallery in London, two in the Tate Gallery and one, a self portrait of 1907, in the Uffizi in Florence which presumably commissioned it as part of its celebrated collection of artists' self portraits. Other pictures may be seen in houses and institutions open to the public.