Durkin began a career in coaching immediately following his playing career. He worked as a
graduate assistant at Bowling Green under new head coach
Urban Meyer in 2001 and 2002, and at
Notre Dame under head coach
Tyrone Willingham in 2003 and 2004. He returned to Bowling Green in 2005, where he coached defensive ends, linebackers, and special teams on the staff of
Gregg Brandon. In 2007, he moved to
Stanford on the first staff of
Jim Harbaugh, where he served for three seasons as the Cardinal defensive ends coach and special teams coordinator. In 2010, Durkin was reunited with Meyer when he joined the
Florida Gators as linebackers coach and special teams coordinator. He remained on Florida's staff when
Will Muschamp took over as head coach in 2010, and in 2013 was promoted to defensive coordinator, replacing
Dan Quinn. Durkin has a reputation as a strong national recruiter and was named the 2012
Rivals.com Recruiter of the Year. On November 22, 2014, Durkin was named interim head coach for Florida's bowl game after the previous head coach,
Will Muschamp, announced he would step down following the regular season. Durkin led Florida to a 28–20 victory in the
2015 Birmingham Bowl against
East Carolina. On January 5, 2015, sources confirmed that Durkin was hired as the defensive coordinator of
Michigan. The hire reunited Durkin with new Michigan head coach Jim Harbaugh. Michigan confirmed the hire on January 8, and announced that Durkin would also coach linebackers. On December 2, 2015
ESPN's
Joe Schad announced that Durkin was expected to be named head coach of the
Maryland Terrapins football team, which was confirmed later that day. On January 2, 2020, Ole Miss announced it had hired Durkin as an assistant to head coach Lane Kiffin, along with
Chris Partridge and Joe Jon Finley. On January 5, 2022, it was announced Durkin would become the new defensive coordinator at Texas A&M under
Jimbo Fisher. On January 31, 2024, Auburn had announced that it had hired Durkin as their next defensive coordinator. On November 2, 2025, Durkin was named Auburn's interim head coach after the firing of
Hugh Freeze, going 1-2. After
Alex Golesh was hired as the program's head coach on November 30, Durkin was retained as defensive coordinator. ==Player death at Maryland and resulting scandal==