[5] The home game and first victory in team history occurred on October 7, 1971, at the Windsor Arena against the Chatham Maroons, winning 4–2 on the back of future NHL goaltender Eddie Mio who made 49 saves.

Finishing sixth place out of eight teams, the Spitfires drew local rival Chatham Maroons in a best-of-seven league quarter-final.

[7] The Spitfires' first playoff game took place on February 23, 1972, in Chatham, Ontario, for a 3–2 win over the Maroons to take a one-game lead in the series.

Their record would put them four points ahead of the second place Welland Sabres and automatically give them a berth into the league playoff semi-finals.

The four-game sweep of the Red Wings allowed Windsor to rest up for the winner of the Chatham Maroons and Welland Sabres, a series just starting.

[15] On March 16, 1974, the Spitfires engaged long time foe Chatham Maroons at the Windsor Arena in the first game of the SOJHL Final.

On March 18, goalie Dennis Thorpe's 40 save performance and third period game winner by Gary Armstrong gave the Spitfires a 2–1 home victory and a lead in the series.

Before a crowd of 5,117 fans, team captain Hugh Mitchell hoisted the Jack Oakes Memorial Trophy to celebrate their playoff victory.

The first team in their way, in the Dudley Hewitt Cup Eastern Canada playdowns was the Wexford Raiders of the Ontario Provincial Junior A Hockey League.

Game five, in Windsor, Ian Campbell would score a late third period tally to break a 2–2 deadlock and send the Spitfires to the league finals.

[21] After a week layoff, the Spitfires were up against a hot opponent and were missing scoring champion John Tavella to a three-games suspension for butt-ending against Detroit.

In a last gasp for air, the Spitfires fought to win a 6–4 decision in Windsor to tie the series at 7 points each and force a final eighth game - winner take all.

Wayne Mills started in net for the Spits, but would be later relieved by back-up Bob Parent when the Generals made it 7–0 at 11:29 of the second period.

Having earned the right to represent the OHL in the 1988 Memorial Cup hosted in Chicoutimi, Quebec, the Compuware Spitfires advanced to the Championship game, where their string of success ended, losing to the Medicine Hat Tigers.

On October 18, 2005, Head Coach Moe Mantha was handed a 40-game suspension and later terminated without pay, for a hazing incident that occurred aboard a bus after a pre-season game versus the London Knights.

On April 6, 2006, the Ontario Hockey League Board of Governors announced the approval of a new ownership group for the Windsor Spitfires, composed of Bob Boughner, Warren Rychel and Peter Dobrich.

Boughner assumed the roles of President, CEO and head coach of the Spitfires, Rychel was named director of player development, and Dobrich the new business manager.

On February 18, 2008, team captain and Calgary Flames prospect[26] Mickey Renaud died of an undetected heart condition[27] in his Tecumseh, Ontario, home.

[38] The OHL Final began with a 10–1 victory for the Spitfires over the Eastern Conference's Brampton Battalion led by stars Cody Hodgson and Matt Duchene.

Their victory marked the first time a team started with two losses in the Memorial Cup round robin and came back to win the championship.

[49] In the aftermath of the championship, the team was met at the Windsor Airport by a large contingent of local fans and was addressed by Mayor Eddie Francis.

At the end of the tournament, the Spitfires acquired defenceman Marc Cantin, forward Stephen Johnston and German goaltender Philipp Grubauer from the Belleville Bulls in exchange for forwards Panik and Austen Brassard, defenceman Paul Bezzo, goaltender Steve Gleeson and a seventh-round pick in the 2012 OHL Priority Selection.

In the league final, the Spitfires made quick work of a highly touted Barrie Colts squad, sweeping them in four games to win their second straight J. Ross Robertson Cup.

They did not need to defeat the Quebec Major Junior Hockey League's Moncton Wildcats in their third and final round-robin game, but did so anyway, winning 4–3 in overtime.

The Spitfires won the game 6–5 in front of a short-lived Canadian Hockey League record of 25,749 spectators, surpassed later that night by the London Knights and Plymouth Whalers at the same venue.

Boughner's new job seemed to be very successful, as he and former Spitfire Peter DeBoer lead the team to the 2016 Stanley Cup Finals, losing to the Pittsburgh Penguins.

On December 4, 2016, the Saginaw Spirit hosted the Spitfires in front of a crowd of over 3,100 people in the closing of Joe Louis Arena in Detroit, Michigan.

[57] The Windsor Compuware Spitfires won the Hamilton Spectator Trophy, the J. Ross Robertson Cup, and were the top-ranked junior team in Canada during the 1987–88 season.

Both the primary logo and shoulder patch designs were collaborations by Marcello Fontana and Shane Potvin, both senior art directors at Hargreaves Stewart.

Domenic Papa previously hosted and provided colour commentary for Spitfires games, alongside Bill Kelso on play-by-play and Brian Trenholm with analysis.