Bekker was born in Oakville, Ontario and began his youth soccer career with the Oakville Blue Stars, winning back-to-back Ontario Cup Championships in 2004 and 2005 and a National Championship in 2004. In 2006, he moved onto the Mississauga Dixie Dominators, where he won the Ontario Cup in 2006 and 2007 adding another National Championship in 2006. In 2007, he also played with Sigma FC, where in March of that year, his team played eight matches in the Netherlands against professional youth academies. His time over there earned him a trial with Ajax’s youth academy, which ended up lasting six weeks until his inability to receive a European work permit led to his return to Canada.

Bekker eventually received interest from colleges in the United States before accepting a scholarship to attend Boston College. During his four years at Boston College, Bekker played in 80 games, starting 79 of those, while scoring 17 goals and adding 22 assists. He picked up several awards on his way including ACC All-Freshman-Team in 2009 and ACC All-First-Team in 2011 and 2012.

Bekker trained with Toronto FC during the summer of 2011, and then trained with Montreal Impact and Seattle Sounders in the Summer of 2012. He had a trial with Crystal Palace in December 2012, before work permit issues led to signing a pro contract with MLS and entering the MLS Draft.

Bekker played in the 2012 CONCACAF Men’s Olympic Qualifying Tournament. On January 18, 2013, he received his first call up by the Canada national team for friendlies against Denmark and United States. Bekker made his senior team debut as a starter against Denmark, the game ended in a 4–0 defeat. On June 27, 2013 Bekker was listed as a part of the confirmed 23-man squad for Colin Miller’s Canada squad for 2013 CONCACAF Gold Cup.

Bekker signed a contract with MLS on January 6, 2013. He was drafted third overall in the 2013 MLS SuperDraft by Toronto FC on January 17, 2013. Bekker made his debut for Toronto on March 2, in a 1–0 away defeat to Vancouver Whitecaps FC.

On January 21, 2015, Bekker was transferred to FC Dallas. He made his debut for Dallas as a substitute for Fabian Castillo on March 14 in a 3–1 victory against Sporting Kansas City.

On July 16, 2015, Bekker was transferred to Montreal Impact in exchange for central defender Bakary Soumaré. Bekker was released by Montreal on December 9, 2016.

Bekker signed with USL side North Carolina FC on February 6, 2018.

In November 2018, Bekker joined Forge FC of the new Canadian Premier League. Bekker would cite the desire of starting for a new club in a new league as motivation for the move. In April 2019, Bekker was named the first captain in team history. On April 27, 2019, he participated in the first ever game in Canadian Premier League history, as Forge hosted York9 FC and battled them to a 1–1 draw. In the 2019 Canadian Premier League season, Forge finished as the runners up in both the spring and fall seasons, qualifying them for the 2019 Canadian Premier League Finals where they faced off against Cavalry FC over two legs. Forge won both games 1–0 to win the North Star Shield and become the first ever Canadian Premier League champions. Bekker also played all four of Forge’s games in the 2019 CONCACAF League, in which they defeated Antigua GFC in the first round but were defeated in the round of sixteen by Olimpia. Bekker finished the 2019 season with five assists, tied for first in the league with five other players. He also scored four league goals, as well as one in the Canadian Championship.