John Holmes was born 29 April 1951, son of Leslie Howard Holmes and Joyce Mary (née Stone). He was educated at Preston Grammar School and Balliol College, University of Oxford, and in 1976, married Margaret Penelope Morris, having three daughters.

Holmes joined the Diplomatic Service in 1973 and served in the following posts: Foreign and Commonwealth Office, 1973-76; 3rd Secretary, then 2nd Secretary, Moscow [Soviet Union], 1976-78; Near East and North Africa Department, FCO, 1978-82; Assistant Private Secretary to Foreign Secretary, 1982-84; 1st Secretary (Economic), Paris [France], 1984-87; Assistant Head of Soviet Department, FCO, 1987-89; seconded to Thomas de la Rue and Company, 1989-91; Counsellor, Economic and Commercial, New Delhi [India], 1991-95; Head of European Union Department (External), FCO, 1995; on secondment as Private Secretary (Foreign Affairs), 1996-99 and Principal Private Secretary, 1997-99, to the Prime Minister [John Major and Tony Blair]; Ambassador to Portugal, 1999-2001; Ambassador to France, 2001-07; Under-Secretary General for Humanitarian Affairs, United Nations, 2007-10.