While still a pupil at Jarrow Grammar School, Miles was a member of a local band called The Influence, which also included Paul Thompson, later drummer with Roxy Music; and Vic Malcolm, later lead guitarist with Geordie. This outfit released the single "I Want to Live" (Orange Records, 1969). Following this he formed The John Miles Set before starting his solo career in 1971.
A 1973 recording by Miles, "One Minute Every Hour" is a favourite with Northern Soul audiences.
Miles signed a recording contract with the Decca UK label in 1975 and issued four albums Rebel (1976), Stranger in the City (1977), and Zaragon (1978). However, John Miles had the most success with singles and released a total of eighteen of them during this era. In addition to "Music", he also charted in the UK with "Highfly" (1975), "Remember Yesterday" (1976), and "Slow Down" (1977). Most of his songs were co-written with the bassist in his backing group, Bob Marshall.
At the peak of his success, in 1976 and 1977, Miles made several appearances on the weekly pop TV show Supersonic. The debut album did receive some attention in the US. Two singles from the debut album reached the US Billboard Hot 100 chart, "Highfly" peaked at No. 68, followed by "Music" which stalled at No. 88. "Slow Down" was his biggest US chart hit, peaking at No. 2 on the disco chart, and at No. 34 on the Billboard Hot 100 in June 1977. It was later featured in the 1979 film, Players, starring Ali MacGraw and Dean Paul Martin.
In the 1980s, Miles continued to record and tour. In 1983 a new radio station in the South of England, Radio Mercury, used parts from the song "Music" for their link jingles. The song itself was played frequently on the station.
Since 1985, Miles participates almost every year in the Night of the Proms, a series of concerts held yearly in Belgium, the Netherlands, Germany, Luxembourg, Poland, Denmark and the United States. Regularly there are also shows in Spain, France, Austria, Switzerland and Sweden. The concerts consist of a combination of pop music and popular classical music (often combined) and various well-known musicians and groups usually participate. Miles always performs "Music", and also sings other songs. In 2009, an album The Best of John Miles at the Night of the Proms was released, which included "Music" and cover versions including "All by Myself", "Bohemian Rhapsody" and "It Was a Very Good Year".
Miles has also toured with Tina Turner since 1987, playing keyboards, guitar and supporting vocals on every one of her tours, and played on several of her albums. He also appeared on Jimmy Page's 1988 album Outrider and subsequent tour, and played Hammond organ on Joe Cocker's album Night Calls (1992). In 1990, Miles participated in the UK heat of A Song for Europe with the song "Where I Belong", which came second.
Miles was also a frequent guest vocalist on albums by The Alan Parsons Project, being featured on Tales of Mystery and Imagination (1976), Pyramid (1978), Stereotomy (1985), and Gaudi (1987), as well as on the Eric Woolfson album Freudiana (1990).
His first DVD, John Miles – Live in Concert was released in 2002. In 2007, Miles performed in Gelsenkirchen, Germany with the German band Pur and sang two songs. One of those songs, "Abenteuerland", Miles sang with Pur in German. The concert is available on the DVD, Pur-Friends-Live-Schalke-2007. In October 2008, Miles began touring once again with Tina Turner. Turner's extensive American-European tour stretched until May 2009. He also toured with Jimmy Page on his Outrider tour with amazing crowd reception taking on Led Zeppelin, Outrider, Yardbirds, and Firm songs.
Miles' son, John Miles Jr., is also a musician. Born in London, he has played with bands including Milk Inc., Sylver, The Urge Fixate.