Timlin started his career with his local club Buncrana Hearts and at Scoil Mhuire, Buncranabefore going on trial with English club Ipswich Town in July 2011, and impressed enough to secure a contract offer from the Tractor Boys.
After 3 seasons with Ipswich reserves scoring 10 goals in 35 games, Timlin's contract came to an end and he made the move back home and went on trial with League of Ireland side Derry City. He impressed Derry boss Roddy Collins enough that he was signed within the week, just prior to the 2014 League of Ireland season. He missed the start of the season through injury but fought his way into the starting eleven following his comeback from injury and kept his place for the majority of the season, even under new manager Peter Hutton as Roddy Collins was sacked not long into the season. He started 18 league games over the season, scoring once, in a 4–2 win over Bohemians. Timlin featured in all four of Derry's Europa League games, scoring in a 4–0 home win over Welsh side Aberystwyth Town in the first qualifying round as his side advanced to face Shakhtyor Soligorsk of Belarus who knocked them out of the competition. He remained an unused substitute in the 2014 FAI Cup Final as Derry lost 2–0 to St Patrick's Athletic. Timlin became one of City's main men in the 2015 League of Ireland season as they had a poor season, finishing seventh in the league after bad form saw them sack manager Peter Hutton and replace him with his assistant Paul Hegarty, as they were dragged into a relegation battle in the last third of the season. He scored many important goals in their relegation fight and finished the season as Derry's top goalscorer with 10 goals in the league from 28 appearances as well as one goal in the FAI Cup vs Edenderry Town and one in the League Cup against Sligo Rovers. He was also sent off twice against Sligo in the league. After his impressive from for Derry, Timlin attracted many clubs, including rivals St Patrick's Athletic and Shamrock Rovers. New Derry manager Kenny Shiels was also trying his utmost to keep Timlin at the club but was admitted it looked unlikely as he was looking to move onto the next step of his career.
On 30 November2016, Timlin returned to Derry City under manager Kenny Shiels on a one-year contract with the option of a second year.
Finn Harps
Timlin signed for Finn Harps on 28 July 2017 and in no time became Finn Harps solution which lead them back to the first division after a 1-year absence and a return to Donegal again