Heneghan joined Chester in August 2014, initially on non-contract terms. On 16 August, he debuted as a half-time substitute against Braintree Town coming on at right back. On 30 August, Heneghan made his first start for Chester, against Gateshead replacing captain Matty Brown. He maintained his place in the squad playing mostly as a right back. On 24 September, Heneghan scored his first professional goal, a 94th-minute winner against Cross-border derby rivals Wrexham. Two days later he an agreed contract until the end of the season. Heneghan switched to his preferred central back position in January, when Chester finally signed right back Ryan Higgins. On 30 March, Heneghan and Higgins signed new contracts until the end of the 2015–16 season. Heneghan finished the season as a first choice centre back playing 44 matches and scoring eight goals, including valuable ones against Stockport County and Southend United in FA Cup matches. Heneghan started the 2015–16 season building a strong partnership in the middle of the defence with the experienced Ian Sharps, but was sent-off in the fifth game of the campaign as Chester lost 5–2 to Woking. On 19 September, Heneghan scored the winning goal against Eastleigh. During the season Heneghan was reported to be attracting interest from clubs in the Football League and in Scotland, though he had not ruled out remaining with Chester.
Motherwell
On 23 June 2016, Scottish Premiership club Motherwell confirmed the signing of Heneghan on a two-year deal. He made his début in a 2–0 home defeat against Rangers in the Scottish League Cup. The defender spent a year in Scotland, playing exactly 50 games in all competitions, scoring one goal in a 2–1 home loss in the Scottish Premiership against Rangers.
Sheffield United
On 31 August 2017, Heneghan signed for Championship club Sheffield United on a three-year contract. He was transfer-listed by Sheffield United at the end of the 2017–18 season. On 3 July 2018, Heneghan moved to Blackpool on a season-long loan. After a difficult start, Heneghan settled into a defence that regularly kept clean sheets and became a fans favourite by the end of the season. On 23 August 2019, Heneghan returned to Blackpool on a loan deal until January. In January, this was extended until the end of the season. Heneghan left Sheffield United at the end of the 2019–20 season, having been released on a free transfer.