The original Windsor Spitfires played in the Ontario Hockey Association from 1946-1953.

After a 17-year hiatus from junior hockey, the modern-day Spits began operations in 1971, playing four years in the Southern Ontario Junior A Hockey League.

In 1975, the team was granted entry as an expansion franchise in the Ontario Major Junior Hockey League (OMJHL), which later became the Ontario Hockey League (OHL). The Spits won their first-ever major junior game on October 2, 1975 in dramatic fashion, rallying from a six-goal deficit to beat the Sudbury Wolves 11-10.

Peter Karmanos (founder and CEO of Compuware) bought the team in 1984 and renamed it the Windsor Compuware Spitfires.

The Compuware Spitfires played in the 1988 Memorial Cup in Chicoutimi, Quebec, losing the championship game to the Medicine Hat Tigers.

When Karmanos sold the team to Steve Riolo after the 1988–89 season, the team reverted back to the Windsor Spitfires name and adopted a new logo and new colours.

On April 6, 2006, the Ontario Hockey League Board of Governors announced the approval of a new ownership group; with Bob Boughner assuming the roles of President, CEO and Head Coach of the Spitfires, Warren Rychel was named Vice-President and General Manager, with Peter Dobrich serving as the club’s Governor.

On December 11, 2008, a new sports-entertainment facility known as The WFCU Centre opened northeast of the intersection of Tecumseh and Lauzon Roads, effectively replacing the 84-year-old Windsor Arena.

The franchise began an historic run during that 2008-2009 season, winning the first of back-to-back Ontario Hockey League Championships and MasterCard Memorial Cup titles – feats duplicated in the 2009-2010 season, as the club won another OHL title before winning its second-consecutive MasterCard Memorial Cup title in Brandon, Manitoba.

On May 9, 2013, John Savage, Stephen Savage and Brian Schwab, owners of Cypher Systems Group, were introduced as new members of the club’s ownership group, as Dobrich sold his share of the franchise.

On July 2, 2015, Boughner accepted a position as assistant coach with the National Hockey League’s San Jose Sharks. The following day, the club announced former Edmonton Oilers assistant Rocky Thompson as its new head coach.

On May 2, 2016, the Canadian Hockey League announced the Spitfires would host the 2017 MasterCard Memorial Cup from May 18-28, 2017.

Thanks to months of planning and hard work, the event was a huge success, both on an off the ice. The Spitfires overcame a 44-day break between their elimination from the Ontario Hockey League playoffs and the beginning of the tournament, going 3-0 in the round-robin before defeating the Erie Otters, 4-3, on Sunday, May 28th, to capture their third Memorial Cup title in nine years and first ever on home ice.