Born in Minnigaff, Kirkcudbrightshire, Mirrlees was educated at the University of Edinburgh (MA in Mathematics and Natural Philosophy in 1957) and Trinity College, Cambridge (Mathematical Tripos and PhD in 1963 with thesis title Optimum Planning for a Dynamic Economy, supervised by Richard Stone). He was a very active student debater. One contemporary, Quentin Skinner, has suggested that Mirrlees was a member of the Cambridge Apostles along with fellow Nobel Laureate Amartya Sen during the period.
Between 1968 and 1976, Mirrlees was a visiting professor at the Massachusetts Institute of Technology three times. He was also a visiting professor at the University of California, Berkeley (1986) and Yale University (1989). He taught at both Oxford University (1968–1995) and University of Cambridge (1963–1968 and 1995–).
Mirrlees and Vickrey shared the 1996 Nobel Prize for Economics "for their fundamental contributions to the economic theory of incentives under asymmetric information".
In 2009, he was appointed Founding Master of the Morningside College of the Chinese University of Hong Kong.
Mirrlees is also co-creator, with MIT Professor Peter A. Diamond of the Diamond–Mirrlees efficiency theorem, which was developed in 1971.
