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Collins scored his first goal in Sutton's 2017–18 campaign in their opening match, a 2–0 win against Leyton Orient.

Remaining as Sutton captain for the 2016–17 season, Collins scored his first goal in the National League when he headed in a corner in a 3–1 victory against Lincoln City at Sincil Bank on 13 August 2016, helping Sutton to earn their first win in English football's fifth tier in 16 years. Sutton supporters unofficially voted Collins player of the month for September 2016 and again (now officially as a re-instituted award) for October 2016.

Collins made his 100th career appearance for Sutton on 3 December 2016 in a 2–1 win against League Two club Cheltenham Town in the 2nd round of the FA Cup. In the 4th round on 29 January 2017, Collins scored a calmly taken penalty to knock out Championship side Leeds United 1–0 and send Sutton through to the 5th round for the first time in the club's 118-year history. On 20 February, Collins captained Sutton when they were defeated 0–2 by Premier League team Arsenal. He finished the season with a tally of eight goals in the league and was named Club Player of the Year.

After being released by Eastleigh, Collins signed for Sutton United at the start of 2015, making 19 league appearances in the second half of the 2014–15 season and scoring his first goal for the club in a 2–1 victory against Basingstoke Town on 11 April 2015. Collins was appointed captain for the 2015–16 season, making 29 full and two substitute league appearances for the U's and scoring a further five goals, leading them to winning the National League South title. He was named in the National League South team of the season.

In May 2013, Collins and Forest Green agreed to the mutual termination of his contract and he moved to Eastleigh.

On January transfer window deadline day on 31 January 2012, Collins signed for Forest Green Rovers on an 18-month contract for an undisclosed fee. Collins made his Forest Green debut on 18 February 2012 in a home win against Gateshead. In July 2012, Collins signed an extension to his contract at Forest Green which would see him stay at The New Lawn until the end of the 2013–14 season.

In January 2011 Holdsworth became manager of League Two side Aldershot Town, and Collins followed his former boss five months later, signing on a free transfer at the end of the 2010–11 season.

After a disappointing 2008–09 campaign, Collins joined division rivals Hampton & Richmond Borough for an undisclosed fee. He spent just three months at the club before being signed by Newport County manager Dean Holdsworth, where he went on to be a key player in the 2009–10 season, as Newport won the Conference South title with a record 103 points.

Collins began his youth career as a scholar at Watford, signing a professional contract with the club in June 2004. However, he failed to impress and was released the following February. Collins joined Havant & Waterlooville F.C. for the rest of the season, quickly impressing the fans and signing a full contract with the club in May 2005. Collins went on to play four seasons with The Hawks, becoming a first team regular and being rewarded with the captaincy for the 2007–08 season. In his first season as captain, Havant made a memorable run in the FA Cup, knocking out Football League sides Notts County and Swansea City to earn a fourth round tie away at Liverpool, in which they twice took the lead before losing 5–2.

James Edward Collins (born 28 September 1984) is an English semi-professional footballer who plays as a defender for and captains National League club Sutton United.