When he graduated from college in 1965, he was hired as an executive vice president at Modern Security Life of Springfield, Missouri, his father's insurance company. He received his Master's degree in business in 1970. After several unsuccessful business ventures (including passing up the opportunity to purchase the American Football League's San Diego Chargers in 1967), he began an oil and gas exploration business in Arkansas, Jones Oil and Land Lease, which became successful. His privately held company currently does natural resource prospecting.
On February 25, 1989, Jones purchased the Cowboys from H.R. "Bum" Bright for $140 million. Soon after the purchase, he fired longtime coach Tom Landry, to that point the only coach in the team's history, in favor of his old teammate at Arkansas, Jimmy Johnson. A few months later, he fired longtime general manager Tex Schramm, and assumed complete control over football matters.
The Cowboys won the Super Bowl at the close of two seasons in 1992 and 1993. Johnson then departed and was replaced by Barry Switzer. During Switzer's tenure, the Cowboys also won the Super Bowl in the 1995 season.
In an online poll from October 8, 2003, Jones was named the least favorite sports personality by Sports Illustrated, in three states (Virginia, Delaware and Texas). He is often vilified by fans who remain bitter at Jones' unceremonious firing of fan-favorite Landry. Some of the fan criticism is due to Jones' high visibility and involvement as the "face of the team" which is in stark contrast to original owner Clint Murchison Jr.
Some Dallas Cowboys fans have expressed their displeasure with Jones and the lack of success in the franchise. This had led to formation of grassroots organizations aimed at displacing Jones from his position.
Jones is the subject of the 2008 book Playing to Win by David Magee. In the book, Jones says he handled the firing of Tom Landry poorly and takes some blame for the disintegration of his relationship with Landry's successor, Jimmy Johnson.
During the early years of Jones' tenure as owner, the Cowboys had one of the highest payrolls in the NFL, and his critics frequently charged that the team's success was not due to Jones' football managerial skills but rather the result of his willingness and ability to outspend other teams. The NFL's implementation of a hard salary cap in 1994, combined with the implementation of a hard salary floor and consistently increasing television revenues (which are shared equally between all NFL teams) have eliminated the ability of any NFL team to significantly outspend its rivals. After their last Super Bowl win in 1995, the Cowboys have endured consistent mediocrity, winning just two playoff games since 1996. In recent seasons, the Cowboys went 8-8 from 2011–13, losing the NFC East title in Week 17 of the season each year to three different divisional opponents. In 2014 the Cowboys won the NFC East for the first time in 5 years after key drafts and free agent signings. 
Jones was fined $25,000 by the NFL for publicly criticizing referee Ed Hochuli after Hochuli made a controversial call in a game between the San Diego Chargers and the Denver Broncos on September 14, 2008. He made comments both to the press and on his radio show, saying Hochuli was one of the most criticized officials in the NFL. This was Jones' first fine by the NFL.
In 2009, Jones was fined $100,000 for violating a gag order on labor issues, commenting that revenue sharing was "on its way out". Commissioner Roger Goodell had issued a gag order for all owners and team executives from discussing any aspect of the pending labor issues. Jones "crossed the line", drawing a "six-figure" fine, sources said, as the commissioner distributed a memo to all 32 owners, along with a reminder that the gag order remains in effect. Goodell did not disclose the specific amount of Jones' fine in the memo.
Jones was the inspiration for the character Baxter Cain (Robert Vaughn), owner of the Dallas Felons, in the 1998 film BASEketball. He had a brief cameo appearance as himself in the 1998 made-for-television reunion movie Dallas: War of the Ewings. Jones also appeared as himself in a 1996 episode of the TV show Coach and in a 2007 television commercial for Diet Pepsi MAX, which also featured then Cowboys head coach Wade Phillips and quarterback Tony Romo. Jones most recently starred in a commercial for Papa John's in which a stunt man performs a dance act. Jones appeared as himself in the seventh season of the HBO series Entourage in 2010, in an episode of the TNT incarnation of Dallas titled "Truth and Consequences", which aired on July 4, 2012, in a series of commercials for the 2012 season of ESPN's Monday Night Football, and in the season 4 premiere of The League. In 2013, Jones narrated a documentary film on former teammate and business partner Jim Lindsey. Jones also appears in a 2013 Pepsi commercial, walking into an elevator filled with three men wearing New York Giants apparel, who look at him with discontent. Jones also appears on the first episode "Go Fund Yourself" of the eighteenth season of South Park, along with several other NFL team owners (Jones is depicted as having huge, bulging chameleon-like eyes).
Jones is the son of J.W. "Pat" Jones and Arminta Jones. He is married to Eugenia "Gene" Jones, and they have three children: Stephen, Charlotte and Jerry, Jr. Stephen (born July 21, 1964) serves as the Cowboys' chief operating officer/executive vice president/director of player personnel. Charlotte (born July 26, 1966) serves as the Cowboys' executive vice president and chief brand officer.Jerry, Jr (born September 27, 1969) is the Cowboys' chief sales and marketing officer/vice president.