Immediately after graduating, Miller was appointed a teacher of English, Latin and Greek in Maybole, Ayrshire; but his tenure of that post was brief. At the end of the year 1897 he returned to the University of Glasgow, having been appointed to a George A Clark Scholarship in Mathematics and Natural Philosophy. As Clark Scholar he conducted tutorial classes both in Mathematics and in Natural Philosophy. He also worked in the Physics and Chemistry laboratories. In 1899 he was appointed Assistant to that gifted teacher, George A Gibson, who was at that time Professor of Mathematics in the Glasgow and West of Scotland Technical College (later to be designated the Royal Technical College, Glasgow, and now the Royal College of Science and Technology, Glasgow). Ten years later, when Gibson was appointed to the Chair of Mathematics in the University of Glasgow, Miller was promoted to be Professor of Mathematics in the College. In that same year he received from the University of Glasgow the degree of Doctor of Science for a thesis on the "Geometry of the Conic and the Triangle." He remained head of the Department of Mathematics in the College until he resigned in 1934, at the age of sixty-three.
Though he published little, Miller was an accomplished mathematician with a special flair for Geometry. As a lecturer he was clear, concise, methodical and deliberate, earning the appreciation and the gratitude of his students. He was a man of principle, strict but always fair as a disciplinarian, respected by all for his integrity, and held in affection by students and colleagues alike. He was elected a Fellow of the Society in 1910.
John Miller came of a brilliant family. He was the eldest of six sons, all of whom had- distinguished careers, graduating in the University of Glasgow before serving their fellowmen in a variety of professions. John never lost his early love for the Classics. He relinquished his post in the College before reaching the normal age of retiral in order that he might have leisure to extend his classical studies and visit the scenes of Greek and Latin historical lore. At the same time he continued his mathematical reading. Throughout his last years of great and increasing bodily weakness his mental powers remained unimpaired. He was always happy in discussing the days of long ago and especially in recalling memories of the university teachers of his undergraduate days.
Miller was a great lover of music and owned a large collection of records of classical music, besides many volumes of complete operas and symphonies.
His wife died in 1928. They had no children.