Harkes is a recipient of the MAC Hermann Trophy, which is awarded to the best college soccer player in the United States.
During his junior and senior years at Gonzaga College High School, Harkes served as the varsity captain.
Ahead of the 2013 NCAA Division I men's soccer season, Harkes signed a National Letter of Intent to play for Wake Forest University.
On August 30, 2013, he made his Wake Forest debut starting and playing 74 minutes in a 1–0 loss against Coastal Carolina.
[16] On March 12, 2017, Harkes made his professional debut, playing a full 90 minutes in a 0–4 loss at New York City FC.
He scored his first goal for United on June 13, 2017, in a U.S. Open Cup match against amateur side Christos FC.
[18] During his second year with United, Harkes lost his starting role to Júnior Moreno and Russell Canouse, making only eight appearances during the 2018 season.
[19] In January 2019, Harkes signed a two-year contract with Scottish Championship side Dundee United, noting that his Dundee-born grandfather had been a supporter of the club growing up.
[30][31] Harkes made his first appearance for his new club on July 8, 2023, coming on as a 68th-minute substitute for Esmir Bajraktarevic in New England's 2–1 loss to New York Red Bulls.
[34] On January 8, 2018, he received a call-up for the United States men's national soccer team for a friendly against Bosnia and Herzegovina.
He is also the son of Cindi Harkes, who played collegiate soccer for Virginia and professionally in the USL W-League for the Maryland Pride and for Sheffield Wednesday Ladies.