Jackson made his international debut for Scotland in the autumn of 2010, coming on as a substitute in the test against the All Blacks. He also came off the bench against Samoa two weeks later, kicking the winning penalty goal in the 80th minute in a match played at Aberdeen, Jackson's home town. Jackson was the starting Fly-Half for Scotland's 2013 Six Nations campaign, but failed to bring the best from Scotland's attacking players. He was dropped halfway through the Championship for Glasgow teammate Duncan Weir.
In the 2013–14 season, Jackson was again a back-up for Duncan Weir for Glasgow and Scotland. In March 2014, it was reported that he would not be offered another contract from Glasgow. As of the 2014–15 season, he has played for English side Wasps in the Aviva Premiership.
In May 2016, it was confirmed that Jackson would be joining Premiership rivals Harlequins ahead of the 2016–17 season.