Towell started his career at Crumlin United and in 2007 moved to Celtic. In November 2010, he made his professional debut coming on as a substitute for Jos Hooiveld in the 57th minute of Celtic's 2–2 draw against Inverness, he provided an assist for Paddy McCourt.
Hibernian (loans)
On 25 January 2011, he joined Hibernian on loan until the end of the 2010–11 season. Towell made his debut a day later, in a 2–0 loss to Rangers. He was at fault for the concession of the second Rangers goal, as a misplaced pass allowed Nikica Jelavić a clear chance to score. Despite this bad start, Towell helped to solidify the Hibs defence during the latter part of the 2010–11 season. Hibs manager Colin Calderwood stated in April 2011 that he hoped to sign Towell for a longer period. Towell said in April 2011 that he received abuse from Hearts supporters in Edinburgh derby matches because he was Catholic. However, he also said that this made him more determined to play better. Towell returned to Celtic at the end of the season, having made 15 starting appearances for Hibs. Towell re-signed on loan for Hibs on 25 August 2011, on a deal due to run until June 2012. He played the first match of his second loan spell only 3 days later, starting as Hibs lost 2–0 to Edinburgh derby rivals Hearts. Towell started to find first-team opportunities limited after new manager Pat Fenlon made several signings in the January transfer window. Two right backs and two central midfielders came in with one other right back going out. However, Fenlon said that once Towell had got his fitness levels up he would be back in the first team picture.
Towell was signed by Stephen Kenny for Dundalk in December 2012, ahead of the 2013 Airtricity Premier Division season. Towell made his League of Ireland debut against Shamrock Rovers on the opening night of the 2013 season and was hugely influential in Dundalk's second-placed finish that year, scoring seven times in 31 league appearances. He also picked up the PFAI Young Player of the Year award. He won back to back league titles with Dundalk in 2014 and 2015 scoring 11 and 25 goals in the respective seasons, and got his first taste of Champions League football with the League of Ireland champions.
On 31 August 2017, he signed for League One's Rotherham on a season-long loan where he helped them regain their Championship status, winning the 2018 EFL League One play-offs. On 31 August 2018 he returned to Rotherham United for a second season-long loan spell. He made 34 Championship appearances scoring 4 times as Rotherham were relegated back to League One.
Salford City
On 31 May 2019 Towell joined Salford City on a two-year contract.
