He began his career with Queen's Park in 2004 where he played in 78 league games, scoring 22 goals in three seasons with the club. During his time at the club, he was voted into the Third Division Team of the Year in 2006–07.
St Johnstone
He joined St Johnstone in the summer of 2007 for one season, where he played in 27 league games without scoring a goal.
Weatherston signed for Dumfries side Queen of the South on 27 August 2008. Weatherston made his debut with a substitute appearance in the 3–1 league defeat at Palmerston against Dundee on 30 August 2008. He scored his first goal for Queens in the following game in a 1–0 victory over Ross County. In the top of table clash at Palmerston against Livingston on 4 October 2008, Weatherston scored his next two goals. The 6–1 victory saw Queens go top of the First Division for the first time in five years. On 19 February 2011 Weatherston scored his first senior career hat trick in the 4–0 win away at Morton. In his three seasons with the club, Weatherston played in 74 league games, scoring 17 goals.
Falkirk
He signed for Falkirk on 10 August 2011, signing a six-month deal until 3 January 2012. He made his Falkirk debut against Partick Thistle three days later. Falkirk won the match 2–1. He scored his first goal for Falkirk on 17 September 2011 in 2–1 win over Dundee. He made 33 appearances in total in season 2011/12, and in the Summer of 2012, signed a one-year extension to his deal. Weatherston's 2012–13 campaign was to be blighted with injury however, not allowing him to get a consistent run in the team. He made 29 appearances, 9 of those coming from the bench. Weatherston was told in May 2013 he would not have his contract renewed by newly appointed manager Gary Holt, and left the club along with Darren Dods, Sean Higgins, Iain Flannigan and Dale Fulton.
Stirling Albion
On 8 August 2013, Weatherston signed for Scottish League Two side Stirling Albion on a one-year deal along with former Falkirk teammate Dale Fulton. He made his debut against Montrose coming on as a substitute in a 2–1 victory. He played a key role in helping Albion gain promotion through the League Two play-offs, teaming up with old Falkirk teammate Jordan Whiteup front, forming a strong partnership. He finished the season having made 36 appearances in all competitions, scoring 9 goals.
On 12 September 2016, the last day of the transfer window, Verdal confirmed the signing of Weatherston, after attempts from the player to be contracted by Norwegian 1st Division side Levanger had failed.
