Wavertree born John Welsh joined Liverpool at the age of 10. He progressed through the ranks, becoming captain of the Reserve Team in the process. Welsh trained with the Liverpool first team squad at their Melwood training ground from the middle of the 2001-02 season.
In the 2002-03 season John Welsh played only one game for the first team - his début match against Ipswich Town on December 4, 2002 in a League Cup fourth round tie at home - when he replaced Vladimír Šmicer in the 83rd minute. Also, John Welsh has been amongst the substitutes for a number of European games.
His first game in Premiership was against Arsenal on October 4, 2003, when he replaced Salif Diao in the 82nd minute, but he couldn't help his team avoid defeat — they lost 2-1, and unfortunately for Welsh, his first act was to be booked for a foul on Ray Parlour. Welsh featured in Liverpool's run to the 2005 UEFA Champions League Final, coming on as a substitute in the round of 16 away tie against Bayer Leverkusen. Liverpool would go on to win the trophy but Welsh was left out of the final match day squad.
After three starts and seven substitute appearances in all competitions for Liverpool, in August 2005, John went on a season-long loan to Championship side Hull City. The club were impressed, and in November 2005 agreed a deal which saw Liverpool take promising young winger Paul Anderson in exchange. The swap took place on 4 January 2006.
However, three minutes into a match against Preston North End on 10 March 2007, Welsh dived into a tackle with Preston's Neil Mellor, a former Liverpool team mate. Welsh was carried off on a stretcher, and it later transpired that he had broken both the tibia and fibula in his right leg, ruling him out for many months.
On 31 December 2007, Chester City announced they would be signing Welsh on loan when the transfer window reopened the following day. He made his Chester debut on 1 January 2008, in a 2–0 home defeat to Grimsby Town, and spent the rest of the month in Chester's starting line-up before returning to Hull.
He joined Carlisle United on 27 October 2008 for an initial one month loan making his debut against Hartlepool United.
In March 2009, he joined Football League Two side Bury on loan and was released from Hull on 2 June 2009.
In July 2009, John Welsh signed a deal with Tranmere. Welsh had a very consistent season for Tranmere, playing the holding midfield role successfully. Welsh also netted 4 goals in his 1st season at Prenton Park, including a volley in the 4-2 victory over Gillingham and a 25 yard strike in a 2-1 home victory over Brighton.