Derrick Walker established the team in 1991 by purchasing leftover assets from the former Porsche Indy programme. The team made an immediate impact by successfully qualifying rookie Willy T. Ribbs at the Indianapolis 500 in their debut season, a milestone as Ribbs became one of very few Black drivers to compete in the race.
In 1992 the team fielded Scott Goodyear on a full-time basis. Goodyear won at Michigan and came agonisingly close to winning the Indianapolis 500 that year, finishing as runner-up. Willy T. Ribbs rejoined the team from the 1993 Indianapolis 500 through the end of the 1994 season, while Hiro Matsushita drove a third full-time car in 1993.
Robby Gordon replaced Goodyear at the start of 1994, racing with Valvoline sponsorship through 1996. Alongside Gordon, Mark Smith showed promise in his 1993 CART rookie season but struggled during 1994. Smith was replaced by Christian Fittipaldi in 1995, who finished second at the Indianapolis 500.
When the CART–IRL split occurred in 1996, Walker Racing chose to enter both competing events. Gordon and Fredrik Ekblom drove in the U.S. 500 while Mike Groff raced in the Indianapolis 500 itself.
Gil de Ferran joined the team in 1997, driving the Valvoline-sponsored car. He finished as championship runner-up that year despite not winning a race. De Ferran remained with the team through 1999, and in that final season scored his first victory for Walker Racing, breaking a drought that had lasted since Robby Gordon's 1995 win at Detroit.
Without a star driver or major sponsorship secured for 2000, the team turned to pay driver Shinji Nakano, who finished 24th in the championship standings. In parallel, Walker entered the Indy Racing League's IndyCar Series in 2000 with rookie driver Sarah Fisher, who posted a career-best finish of second place at Homestead-Miami Speedway in 2001.
Nakano was replaced in the CART programme in 2001 by fellow Japanese driver Tora Takagi, who brought Pioneer Electronics sponsorship and managed modestly better results, scoring ten top-ten finishes across two seasons. An attempt to field Oriol Servia at the 2002 Indianapolis 500 ended when Servia failed to qualify.
Takagi departed for the IRL in 2003, and Mexican driver Rodolfo Lavin joined with Corona sponsorship while Darren Manning drove a second car full-time, finishing ninth in the championship. In 2004, as the series rebranded as the Champ Car World Series, Brazilian Mario Haberfeld drove the team's single full-time entry.
Late in 2004, Australian businessman Craig Gore bought into the team, steering it toward an Australian identity. The 2005 season brought Aussie Vineyards sponsorship and a return to two full-time cars, with Australian rookie Marcus Marshall joining veteran Alex Tagliani. Will Power made his Champ Car debut in a third car at the 2005 Lexmark Indy 300 in Australia and replaced Marshall for the season finale.
Tagliani and Power continued together in 2006. For 2007, Simon Pagenaud — the reigning Champ Car Atlantic Series champion — replaced Tagliani. Power had an outstanding 2007 campaign, winning two races including the season opener in Las Vegas, the team's first victories since de Ferran's 1999 win. Despite early indications that Walker was preparing for the IRL IndyCar Series in 2008, the team ultimately announced in March 2008 that it could not secure adequate funding after sponsor Aussie Vineyards moved to KV Racing. Walker Racing made a brief 2008 appearance through a joint effort with Vision Racing at Edmonton to run Paul Tracy.
In 2009, Walker fielded Stefan Wilson for a partial season in Indy Lights.
In 2011, Derrick Walker partnered with Team Falken Tire to field a Porsche 997 GT3-RSR in the American Le Mans Series GT class. The team claimed its first ALMS victory at the 2011 Mid-Ohio Sports Car Challenge, where heavy rain gave Falken's superior wet-weather tyres a decisive advantage. Drivers Wolf Henzler and Bryan Sellers took the win after Henzler charged from seventh to first in a single post-safety-car lap before red flags ended the race.
The team, competing as Team Falken Tire, continued in sports car racing through the United SportsCar Championship until Falken Tire withdrew from the series at the conclusion of the 2015 season.
Separately, in 2012 Derrick Walker returned to IndyCar as team manager for Ed Carpenter Racing, operating from the Walker Racing facility and using its equipment and personnel.
On 20 November 2016, the team was put up for auction after a year-long failed search for a replacement sponsor. Following the auction's completion on 6 December 2016, Walker Racing was officially listed as defunct.
Walker Racing's 25-year run touched several chapters of North American open-wheel and sports car history. The team helped launch careers including those of Gil de Ferran, who went on to win two CART championships with Team Penske, and Will Power, who became a multiple race winner and eventually an IndyCar champion. The team's role in qualifying Willy T. Ribbs at Indianapolis in 1991 also carries lasting historical significance in the sport.