Born in Toronto, Ontario, Wekerle spent a year studying at York University before dropping out and taking a job as a phone clerk at the Toronto Stock Exchange. He subsequently joined First Marathon, rising to become head trader for the firm. In this capacity, he was one of the key figures in Rogers Communications' takeover of Maclean-Hunter in 1994.
He left First Marathon in 1995 to join Griffiths McBurney and Partners (GMP). In his role with GMP as vice-chairman of trading, he was closely involved with the 1997 initial public offering of Research in Motion.
In 2010, Wekerle experienced a bout of depression after his then-wife Lea-Anne died of a heart attack. His behaviour became increasingly erratic over the next several months; at a charity fundraising roast for Newcap Broadcasting CEO Rob Steele that summer, he drunkenly interrupted host Rex Murphy, and in October he arrived drunk at a hotel in Little Rock, Arkansas, and allegedly engaged in rowdy and disorderly behaviour. A valet with the hotel filed a lawsuit against Wekerle in 2013, alleging that he had suffered a permanent injury as a result of Wekerle's behaviour. Wekerle left Griffiths McBurney in 2011 by mutual consent, receiving a severance package in return for agreeing to a non-compete clause.
Wekerle launched his own merchant banking firm, Difference Capital, in 2012 to invest in technology startups. His investments through Difference Capital include the film and television studio Thunderbird Films, the data analysis firm Appinions, the medical technology firm BrainScope, the social media management service HootSuite, and the technology firm Vision Critical.  In 2014, he announced the launch of a new business incubator in the Waterloo Region that would offer venture capital funding to new tech startups. He subsequently began buying high-tech commercial buildings in Waterloo, a number of which had previously been owned by BlackBerry.
He was announced in March 2014 as one of two new Dragons, along with restaurateur Vikram Vij, who would be joining Dragons' Den in its ninth season following the departures of Kevin O'Leary and Bruce Croxon. In one of his first dragon deals on the series, he invested in Covergalls, a new line of workwear designed for women in industrial jobs.
Separately from Difference Capital, he is a partner in the Canadian franchise expansion plans of Mark Wahlberg's Wahlburgers chain of restaurants, and purchased El Mocambo, a live music venue in Toronto.
In 2013, he was a participant in the Humour Me Comedy Classic, a charitable event in which business executives train to perform stand-up comedy routines as a fundraiser for Toronto's Hospital for Sick Children. He is also a sponsor of "Wekfest" and "Wektoberfest", annual charitable fundraising music festivals in Waterloo.
He was married twice, his first marriage ended in divorce while his second wife Lea-Anne passed away in 2010.
He lives part-time in Caledon, Ontario.
Wekerle’s Porsche 918 Spyder burst into flames at the Esso gas station on 28 September 2014 in Caledon while he was filling up his gas tank. Some gas overfilled, which caused the explosion. Nobody was hurt during the occurrence.
- "The rise and fall and rise of Michael Wekerle: A second act for Bay Street’s wild child". Canadian Business, October 15, 2014.
- "Top trader ends First Marathon run: Michael Wekerle to become partner at Griffiths McBurney". The Globe and Mail, August 31, 1995.
- "The Oracle of Bay Street: finance bad boy Michael Wekerle is back, and his new firm is already the talk of Toronto". Toronto Life, October 16, 2013.
- "Griffiths McBurney now a major stock market player". Hamilton Spectator, August 9, 1996.
- "Dragons' Den banker Michael Wekerle buys BlackBerry real estate". CBC News, October 15, 2014.
- "Canadian millionaire Michael Wekerle sued for ‘drunken escapade’ in U.S.". canada.com, October 25, 2013.
- "Wekerle exits GMP Capital; lauded as a trader without peers". The Globe and Mail, August 25, 2011.
- "TriNorth with a Difference". National Post, April 10, 2012.
- "Wekerle Joins ‘Maple Syrup Mafia’ to Fund Tech". Bloomberg.com, December 4, 2014.
- "$200-million venture capital fund coming to Waterloo". The Record, April 17, 2014.
- "There will be new dragons in the den". Calgary Herald, March 15, 2014.
- "Covergalls gets snapped up". National Post, October 20, 2014.
- "Dragons' Den star plans Wahlburgers expansion in Ontario". Toronto Star, November 13, 2014.
- "Dragons’ Den cast member Michael Wekerle buys El Mocambo". CityNews, November 6, 2014.
- "Event raises $1-million for SickKids; Third annual humour me comedy classic". National Post, November 16, 2013.
- "Dragons' Den star Michael Wekerle buys Toronto's El Mocambo for $3.7M". Business News Network, November 7, 2014.
- "Michael Wekerle thankful no one hurt after Porsche Spyder bursts into flames". Caledon Enterprise, October 9, 2014.