Starting his career with Fulham, making his debut in 1963 and 149 appearances over six years, Dempsey was signed for West London rivals Chelsea by Dave Sexton in January 1969 for £70,000. He made his Chelsea debut against Southampton in February that year and established himself in the side for the remainder of the 1968-69 season.
Dempsey featured in the successful Chelsea side of the early 1970s, winning the FA Cup with the club in 1970, playing in both fiercely-contested final matches against Leeds United as his side eventually ran out 2-1 winners. A year later, the Cup Winners' Cup was added with a win against Real Madrid in another replay in Athens, in which Dempsey scored the winner from a corner (one of only five goals he scored for the club) as Chelsea won 2-1. He won a number of international caps for the Republic of Ireland (he qualified to play for Ireland through his parents).
He had no further success with the club, but remained during the turbulent later 1970s, and eventually left in March 1978 with the club by then in Division Two, and moved to the Philadelphia Fury of the NASL, playing alongside fellow ex-Chelsea star Peter Osgood. In 1979, he was voted the NASL's defender of the year, beating Franz Beckenbauer into second place.
He was appointed player-manager of Dundalk in August 1983 [http://www.nasljerseys.com/Players/D/Dempsey.John.htm but only departed by mutual consent in March [http://www.nasljerseys.com/Players/D/Dempsey.John.htm.
He also had spells managing Maidenhead and Egham Town before retiring from the game in 1984.
He is now involved in local charity work and recently attended the tributes to Peter Osgood at Stamford Bridge following the latter's death.
He currently works with adults with autism and learning difficulties in a daycentre in the London Borough of Barnet. John has been a care worker in the area for a number of years.