A genuine key position prospect, Henderson was trialed at various key positions in his debut season including forward, defensive and ruck roles. He played a total of fifteen senior matches for the Lions in 2008 and 2009.
Carlton
At the end of 2009, Henderson was traded to the Carlton Football Club. Brisbane exchanged Henderson and its first round draft pick for a second round draft pick and star full forwardBrendan Fevola, who was being traded away from Carlton for disciplinary reasons. Henderson made his debut for Carlton in Round 1, 2010 against Richmond, and he kicked three goals in the Blues' second round game against his old team. Throughout his first season for Carlton, Henderson played nineteen matches, and was played primarily at centre-half forward; but through the first half of 2011, Henderson struggled to gain regular selection as a forward. In mid-2011, Henderson was moved to full-back – mostly out of necessity, as the Carlton defense was hit with a number of injuries at the time. However, Henderson was sufficiently impressive in the role that he held his place as a key defender, either full-back or centre half-back, for the rest of the season. In a 2012 interview, Henderson cited his career highlight as "...last year’s Elimination Final – my first winning-final for Carlton," During the 2012 AFL home and away season Henderson played the early parts of the season in the backline with injuries hindering his performance. During the midpoint of the season Henderson opted to have surgery to fix a groin injury. Under new coach Mick Malthouse coming in to replace former coach Brett Ratten for the 2013 AFL Home and Away season, Henderson started the season as a backman and showed promising signs, keeping the West Coast Eagles' Josh Kennedy goalless in Round 4. At the end of the 2013 Toyota AFL season, Henderson finished 3rd in Carlton's best in fairest, after winner Kade Simpson and Andrew Walker. In the 2014 Home and Away season, Henderson proved to be utilised as a forward where though his season was derailed by an injury during the last 6 weeks kicking 28 goals in 17 matches proved to be his best goal to game ratio along with 5.2 marks a game. In August 2015, Henderson requested a trade from the club at the end of the season, he expressed his desire to play the remaining three matches of the season, but was ruled out by Carlton due to his desire to leave the club. In October, Henderson was traded to the Geelong Football Club.
Geelong
Henderson become a consistent part of Geelong's defence, however from 2019 he struggled to play at the AFL level. After 54 games for Geelong, he was delisted at the end of 2019. But received a reprieve, after being selected with pick #35 in the rookie draft.