Hughes started his career at Arsenal, with whom he won the FA Youth Cup in 1994. He then made 16 first team appearances to earn a winners medal as Arsenal won the 1998 Premier League title. Hughes' highlight for that season was scoring twice as Arsenal defeated Chelsea 2–0 at home. He also made 6 appearances in Arsenal's FA Cup run that season, including the semi final against Wolves, but was left out of the squad for the 1998 FA Cup Final as they clinched the double. Another highlight was a 25-yard last minute equaliser against Leicester City at Filbert Street the following season. Altogether with Arsenal he made 76 senior appearances with 40 of them as a substitute, and scored 7 goals.