Howe spent most of his playing career at West Bromwich Albion, joining the club as a youth in 1952, and making his debut in 1955. A full back, he played nearly 350 games for the Baggies in twelve years, as well as becoming a regular in the England team; he played in the 1958 World Cup, and won 23 caps in total.

Howe was signed by Billy Wright's Arsenal in 1964, and was made club captain. However, in March 1966 he broke his leg playing against Blackpool and never recovered well enough to play in the first team again. Howe retired from playing and became Arsenal's reserve team coach under Bertie Mee, then stepping up to first team coach after the departure of Dave Sexton in 1968. Arsenal won the Double in 1971 with Howe playing a crucial role, but not long after he returned to his old club, West Bromwich Albion, as manager.

Howe's tenure at WBA was not a success, the club were relegated to Division Two in 1973, and Howe moved on to coach Galatasaray, Turkey and Leeds United, before rejoining Arsenal in 1977 as head coach, under Terry Neill. He also became part of the English national side's coaching setup.

After Neill's sacking in December 1983, Howe became Arsenal manager. Despite introducing young players like Tony Adams, David Rocastle and Niall Quinn to the team, his tenure was marked by a further lack of success, and he resigned in March 1986, after reports circulated that the board were looking to replace him with Terry Venables (though in the end George Graham succeeded him).

Howe later joined Wimbledon as assistant to Bobby Gould, and there he helped mastermind the Dons' famous 1988 FA Cup victory over Liverpool. Howe also has spells managing QPR between 1989 and 1991, and Coventry City (as caretaker manager) in 1992. Howe also moved into journalism and broadcasting, becoming a pundit for Channel 4's coverage of Serie A.

Howe returned to coach England under Terry Venables during the mid-1990s (including Euro 96), and returned to Arsenal for a final time in 1997 as a youth team coach. He retired from coaching in the summer of 2003, though currently he occasionally writes as a pundit for BBC Sport's website.