Hunter jõudis teenistusse 1954. aastal ning sellega vahetati kiiresti välja esimese põlvkonna hävitajad, nagu Gloster Meteor ja de Havilland Venom. Hunter sobis hästi päevasteks lendudeks, öösiti hakati kasutama hävitajat Gloster Javelin. Lennukit arendati aja jooksul, uuematel mudelitel olid võimsamad mootorid ja suuremad kütusepaagid. Huntereid kasutati ka RAF-i formatsioonlendudeks, Black Arrows lennutas formatsioonis rekordilised 22 Hunterit. Hävitajat eksporditi üle maailma, see oli kasutusel 22 riigi lennuvägedes.
1960. aastatel jõudis RAF-i kätte ülehelikiiruseline English Electric Lightning ning Hunterit hakati kasutama pigem luureotstarbel või hävitus-pommituslennukina. Kaheistmelised mudelid olid taustaülesannetes ja väljaõppes RAF-is ja Suurbritannia mereväes kasutusel kuni 1990. aastateni. Hunter on 2022. aasta seisuga veel kasutusel Zimbabwe õhuväes.
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