Murray’s first professional fight took place in September 2003 with a 4 round points win over journeyman Peter Buckley. Over the next two years Murray was busy in the ring scoring 15 more wins in 15 fights before in December 2005 defeating Ignacio Mendoza for the WBC World Youth lightweight title. He made one defence of his title against Moebi Sarouna and scored decent wins over Ben Odamattey and Lorenzo Bethea before defeating Dean Hickman at the Ice Arena in Nottingham for the English title. In October 2006 he was awarded the prestigious young boxer of the year award at a ceremony held in London, an award previously held by the likes of Ricky Hatton, Frank Bruno and Barry McGuigan.
Following the Hickman victory, Murray fought twice more against journeyman opponents before meeting Salford boxer Lee Meager for the vacant British lightweight title in July 2008. He won the belt after the referee stopped the fight in the 5th round. Following the fight Meager, a promotional stablemate, announced his retirement. The first defence of his title was made on 17 January 2009 at the Robin Park Centre in Wigan. Murray managed to keep hold of the belt after scoring an 8th round stoppage over Aberdeen’s Lee McAllister.
Murray’s second defence of the title on 13 June 2009 against Stoke fighter Scott Lawton ended before it had even begun when Murray weighed in for the contest 2oz overweight. Despite efforts to get down to the lightweight limit, Murray was unable to shift the weight and was stripped of the belt. The contest with Lawton still went ahead and resulted in a sixth round stoppage for Murray ensuring that he was still undefeated but no longer a champion. As punishment for failing to make the weight in a championship contest Murray, his trainer Joe Gallagher and his manager Mike Marsden were each fined £1500 by the British Boxing Board of Control.
Murray reclaimed the belt on 3 October 2009 after scoring a fourth round stoppage against former British and European champion Jonathon Thaxton at the Altrincham Leisure Centre. He had his fourth official British title fight on 7 May 2010 against Welsh boxer Gary Buckland this time in Widnes. The fight was also for the vacant European title and resulted in an 11th round stoppage win for Murray who was also able to keep his Lonsdale Belt for good. Murray having won the belt outright chose to vacate in order to defend his European crown with Gavin Rees winning the vacant title against John Watson on 6 November 2010.
Murray made the first defence of the European title on 25 September 2010 against the Ukrainian boxer Andriy Kudryavtsev at the Robin Park Arena in Wigan. Kudryavstev had previously fought for the title in 2009 losing to Anthony Mezaache in 12 rounds and had held a number of titles including the Ukrainian national title and the European External Union title. Murray wore down his opponent to score a 9th round stoppage after a high tempo contest. Speaking after the fight Murray said that he knew the fight would be tough after watching Kudryavstev on tape and said that now he wanted to fight the top guys in the lightweight division saying he’d love a “world title shot before Christmas”. Murray’s next fight however was to be on 2 April 2011, traveling to London’s York Hall to defend against Spanish champion Karim El Ouazghari. Both fighters were warned and deducted a point during the fight which Murray eventually won on points over the 12 round distance. The fight against El Ouazghari was Murray’s first since joining up with promoter Frank Warren and was described by some as a “scrappy” performance. Murray summed up by saying “It wasn’t my best fight, it was like having my debut again. I have cleaned up at domestic and European level and I am looking at moving on”. Warren himself said that he’d like to see a fight between Murray and Kevin Mitchell in the future saying “the fans would like to see, but the bottom line is that John is the champion and it’s all about what he wants to do.”
Murray vacated the European belt in order to fight Kevin Mitchell who was not eligible to challenge for the title due to suffering a loss in his preceding fight with Michael Katsidis. Murray’s trainer Joe Gallagher said that John should have been fighting for a world title but as the fight wasn’t mandated then beating Mitchell would be a sure way of getting noticed. Mitchell himself had said that the fight represented a “last chance saloon” for him as the fight with Katsidis had resulted in a third round stoppage. Mitchell had cited “personal problems” as having marred his preparation for that fight.The two met at the Echo Arena in Liverpool on 16 July 2011 with Murray suffering a first career defeat via stoppage in the 8th round. Mitchell had hurt Murray in the 7th round and finally scored a knockdown in the 8th before the referee stepped in to call a halt to the fight in what was described as a “superb” contest.
On 7 October 2011 it was confirmed that despite a first career defeat in his previous fight Murray would take on Brandon Rios for the WBA Lightweight title on 3 December in New York City. Murray lost the fight by TKO in 11th round However, Ríos was overweight and was subsequently stripped of his title and had to pay Team Murray $20000 from his purse. The vacant WBA Lightweight title is only able to be won by Murray.