Henderson spent four years as the goalkeeping coach at
Cork City. When the manager's job at neighbouring
Cobh Ramblers became available in 2004, he became the first member of his family to become a senior manager. He made his managerial bow at
Finn Park on 4 September. He guided the club to third place in the First Division table in
2005, their highest league placing since 1999, and fourth place the following season before delivering the club their first ever piece of silverware when he guided Cobh Ramblers to the
First Division title in
2007. Cobh were relegated in
2008 from the
Premier Division and Henderson took up the manager's post at Waterford United in December 2008. He led the club to the final of the League Cup and the semi-finals of the FAI Cup in 2009, and to the promotion play-offs the following season. However, after an indifferent start to the following season, in May 2011 Henderson was sacked by the Blues. In October 2015, he re-joined
Cobh Ramblers on new three-year contract and the following season he guided Ramblers to Munster Senior Cup victory and a third-place league finish. Ramblers reached the final of the EA Sports Cup in 2018 when they lost 3–1 to
Derry City in a game played in Derry. With the side struggling in the league, Henderson left Cobh in June 2019. He immediately became Head of Youth Development at
Shelbourne in a position he held until April 2021. On 24 November 2022, Henderson made his return to first-team management when he was appointed manager of
Longford Town. Longford finished in eighth place of ten teams at the end of the 2023
League of Ireland First Division season. The following season began very poorly with the side bottom of the table and winless after eight games when Henderson departed as manager on 13 April 2024. In June 2024, Henderson was appointed manager of
Munster Senior League side,
Cobh Wanderers. ==Honours==