Gallagher was first called up to the senior team by Brian McEniff for winter training in 2003. He made his senior debut for Donegal in 2004. That year his team made it to the Ulster final but were defeated by Armagh. 2005 was unsuccessful. Donegal reached the 2006 Ulster Senior Football Championship Final and he played in that match at Croke Park. In 2007, he was part of the Donegal team that won the county's first National Football League title. They defeated Mayo in the final. He was the caption that day. Alongside Glenswilly teammate Ciaran Bonner, he was dropped by manager John Joe Doherty over a breach of discipline ahead of the 2009 All-Ireland Senior Football Championship qualifier game against Carlow. By 2011, he had no career and was presumed finished. He was 28 years of age and a peripheral figure in manager Jim McGuinness's first season in charge. Then, quite suddenly, he became a linchpin of McGuinness's Donegal midfield, winning his first Ulster Senior Football Championship in 2011. He won his second Ulster SFC in 2012. Though he did not play in the final against Down, he featured in earlier rounds and contributed a point in the quarter-final victory over Derry. He was then part of the Donegal team that advanced through the 2012 All-Ireland Senior Football Championship. The best performance of his career with Donegal came against Cork at Croke Park in the All-Ireland semi-final; indeed, it is widely regarded as one of the all-time best in team history. He scored a point against Mayo in the 2012 All-Ireland Senior Football Championship Final as Donegal claimed the Sam Maguire Cup. He won an All Star and attended the Football Tour of New York. He also started for Donegal in the 2014 All-Ireland Senior Football Championship Final. He won his third and final Ulster SFC in 2014. Under the management of McGuinness's successor, Rory Gallagher, he continued to feature for his county team. However, he was bedeviled by injuries. On Valentine's Day in 2017, he attended training at Convoy — it was upon the Convoy turf that he broke down for the final time and relinquished his status as an inter-county footballer. Gallagher later described Gallagher as "very disappointed... He wanted to give it a go... He got the back re-scanned and tried to build it up". He announced his retirement from inter-county football at the age of 33 on 20 February 2017.
Business venture
In conjunction with teammate Michael Murphy, Gallagher opened the sports store "Michael Murphy Sports and Leisure" in Letterkenny in August 2014.