In February 1976, Jack joined the staff at Palouse neighbor Idaho, but a month later became the head coach at Cal State-Northridge, a Division II program in Southern California. The family moved after John’s freshman year at Pullman High School to the San Fernando Valley, where he played his final three years of football at Granada Hills High School in Granada Hills, under head coaches Jack Neumeier and Tom Richards. Despite missing five games with a knee injury as a senior, he ended his high school career with 5,711 passing yards and 49 passing touchdowns, and was named to the PARADE All America High School Football Team, along with future NFL stars, quarterback Dan Marino and running back Eric Dickerson.

In 1979, he enrolled at Stanford University, where he played football and baseball. In his senior season in 1982, Stanford was 5-5 and needed to win its final game, the Big Game against California, to secure an invitation to the Hall of Fame Classic bowl game. With two minutes remaining in the game, Stanford was down 19-17 and had 4th-and-17 on their own 13-yard line. Elway completed a 29-yard pass and drove the ball downfield to the 35-yard line, where Mark Harmon kicked what appeared to be the winning field goal. However, the clock had four seconds remaining, so Stanford had to kick off. What followed is now simply known as “The Play”, in which Cal players lateraled the ball, rugby-style, five times – two of them controversial – and scored a touchdown to win the game, 25-20. Elway was bitter about the game afterward, stating that the officials “ruined my last game as a college football player.” Stanford athletics director Andy Geiger said the loss cost Elway the Heisman Trophy. Twenty years later, Elway came to terms with The Play, saying that “each year it gets a little funnier.”

Although Elway never led his team to a bowl game, he had an accomplished college career. In his four seasons (1979–1982) at Stanford, he completed 774 passes for 9,349 yards and 77 touchdowns, with 39 interceptions, while also scoring 5 touchdowns rushing the ball. Stanford had a 20–23 record during his tenure. Elway’s 24 touchdown passes in 1982 led the nation, and at the conclusion of his career, he held nearly every Pacific-10 record for passing and total offense. He won the Pac-10 Player of the Year honors in 1980 and 1982, was a consensus All-American, and finished second in Heisman Trophy balloting as a senior. In 2000, Elway was enshrined in the College Football Hall of Fame. In 2007, Elway was ranked #15 on ESPN’s Top 25 Players In College Football History list. He passed for over 200 yards in 30 of his 42 collegiate games.

Elway told the Colts in December 1982 that he did not want to play for the team, and later told the Colts that he wanted to play on the West coast or for the Dallas Cowboys or Miami Dolphins. After unsuccessfully attempting to negotiate a private agreement with the Colts in which Elway would cite his alleged desire to remain on the West coast to explain the team trading him, Elway publicly threatened to join the Yankees full-time if the Colts did not trade him; Demoff wrote in his journal, published three decades later, that “he would be a garbage collector before he’d play for Baltimore.” Elway’s refusal to join the Colts was controversial— Pittsburgh Steelers quarterback Terry Bradshaw denounced him, stating “you should play baseball … he’s not the kind of guy you win championships with”—but many other NFL teams began negotiations with the Colts for the quarterback. One possibility was trading Elway for the San Francisco 49ers’ Joe Montana, whose team had had a poor season in 1982. Another was a trade with the San Diego Chargers, which was negotiating a new contract with its star quarterback Dan Fouts. The New England Patriots were interested, but the Colts did not wish to trade Elway to a team in the same division. The Los Angeles Raiders almost traded for Elway the day before the draft, but the Raiders could not complete a required trade with the Chicago Bears.

In the 1983 NFL Draft, Elway was selected as the first overall pick by the Baltimore Colts. Elway was wary of playing for the Colts, among the worst teams in the league at the time, and his father advised him against playing for head coach Frank Kush, who had a reputation as a harsh taskmaster. While Elway preferred football, his agent Marvin Demoff later stated that baseball was “a true option” for him at the time. The possibility gave Elway leverage in negotiations with the Colts.

Worried that the Colts would waste their pick, team owner Robert Irsay began negotiating with the Denver Broncos before the draft. His team was interested in offensive lineman Chris Hinton, who the Broncos had chosen as the fourth pick in the first round. On May 2, Irsay and Accorsi agreed to trade Elway for Hinton, backup quarterback Mark Herrmann, and a first-round pick in the 1984 Draft, which turned into offensive lineman Ron Solt. The Colts controversial relocation to Indianapolis the following year would later prove to somewhat vindicate Jack Elway’s concerns, and that franchise would largely struggle until the arrival of Peyton Manning during Elway’s last season as a player.

Elway married Janet Buchan, who attended Stanford University and competed on its swimming team, in 1984. They separated in 2002 and divorced in 2003. They have four children: Jessica, Jordan, Jack, and Juliana.

In the 1986 season, Elway led the Broncos to Super Bowl XXI, after defeating the Cleveland Browns on a famous possession at the end of the fourth quarter that became known as “The Drive”. (In a span of 5 minutes and 2 seconds, Elway led his team 98 yards to tie the game with 37 seconds left in regulation. The Broncos won the game in overtime.) Elway and the Broncos started out the Super Bowl against the New York Giants very well, building a 10–7 lead and then driving to the Giants 1-yard line in the second quarter. However, the Broncos lost five yards on their next three plays and came up empty after kicker Rich Karlis missed the field goal attempt. From that point on, the rest of the game went downhill for the Broncos. Elway was sacked in the end zone for a safety on the Broncos ensuing possession, cutting their lead to 10–9. Then in the second half, the Giants scored 30 points and ended up winning the game 39–20. Still, Elway had an impressive performance, throwing for 304 yards and a touchdown, with one interception, while also leading Denver in rushing with 27 yards and a touchdown on the ground.

In the 1987 season, Elway was selected to start in the American Football Conference’s (AFC) Pro Bowl team and won the NFL Most Valuable Player Award. He went on to once again lead the Broncos to a victory over the Browns in the AFC title game, earning their second consecutive Super Bowl appearance, this one against the Washington Redskins. The game started out very well for Denver, and they built up a 10–0 lead by the end of the first quarter. At the time, no team had ever overcome a 10–0 deficit in the Super Bowl. But in the second quarter, the Redskins suddenly stormed back with a record 35 points, and ended up winning Super Bowl XXII 42–10. Elway did have a few highlights. His 56-yard touchdown pass to Ricky Nattiel after just 1:57 had elapsed in the game set a record for the fastest touchdown in Super Bowl history, at the time. He also became the first quarterback ever to catch a pass in the Super Bowl, recording a 23-yard reception from halfback Steve Sewell on a halfback option play. With a porous defense unable to stop the Redskins offense, Elway was forced to take more risks on the offensive end. As a result, Elway’s performance was rather disappointing: just 14 out of 38 completions for 257 yards and one touchdown, with three interceptions.

After recording an 8–8 record in 1988, Elway once again led his team to the Super Bowl after the 1989 season, with yet another win over the Browns in the AFC championship game, going on to face the San Francisco 49ers in Super Bowl XXIV. However this game ended even worse for the Broncos than their previous Super Bowl losses. San Francisco blew out Denver 55–10, the most lopsided score in Super Bowl history. Although Elway scored the only touchdown for his team on a three-yard run, his performance was abysmal: 10 out of 26 completions for 108 yards with no touchdown passes and two interceptions. But he didn’t try to hide from the media after the game or downplay his dismal performance. And when he was asked if he wanted to go back to the Super Bowl after three losses, he responded that he wanted to go back every year, even if his team kept losing. Still by this point, many doubted that he would ever win a Super Bowl in his career.

Elway owned five auto dealerships, called John Elway Autos, in the Denver area. He sold them to AutoNation Inc. in 1997 for $82.5 million. In December 2006, Elway ended a nine-year licensing agreement with AutoNation, removing his name from Denver-area dealerships. At the time, Elway said the move could allow him to get back into the auto business under his own name. He still owns two Toyota Scion dealerships, one in Manhattan Beach, California and another in Ontario, California, a Chevrolet dealership in Englewood, Colorado, and a Chrysler Jeep dealership in Greeley, Colorado. Elway acquired a Cadillac franchise from Sonic Automotive in 2014.

In the 1998 season, the Broncos repeated this feat and Elway was named MVP of Super Bowl XXXIII, throwing for 336 yards and one touchdown with one interception, while also scoring a rushing touchdown in Denver’s 34–19 win over the Atlanta Falcons. It was his last game, other than the 1999 Pro Bowl.

On May 2, 1999, at the age of 38, Elway announced his retirement from professional football. Elway is regarded as one of the top quarterbacks ever to play the game. He has one of the best winning percentages in league history (148–82–1), and was tied for the second-most Pro Bowl selections for a quarterback (nine) at the time of his retirement. Elway played in 22 postseason games with the Broncos, 21 as a starter, and led the team to victory in 14 of them. In those games he threw for 4,964 yards and 27 touchdowns, with 21 interceptions, while also rushing for 461 yards and 6 more scores. He is currently 9th all time in passing yards , 10th in passes completed, , and 12th in passing touchdowns . His four total rushing touchdowns in his Super Bowl games are the most ever by a quarterback. He is also the second player ever to score a rushing touchdown in four different Super Bowls (running back Thurman Thomas was the first).

On September 13, 1999, Elway’s number 7 jersey was retired by the Denver Broncos during halftime of a Monday Night game against the Miami Dolphins; that same night he was inducted into the Denver Broncos Ring of Fame. (Craig Morton, his direct predecessor in Denver, also wore number 7 and is in the Ring of Fame alongside Elway). He was the first Broncos player to have the five-year waiting period waived. Also in 1999 he was inducted into the Colorado Sports Hall of Fame.

Also in 1999, Elway was ranked number 16 on The Sporting News’ list of the 100 Greatest Football Players, the only player to have spent the majority of his career with the Broncos to make the list (Willie Brown, who began his career with the Broncos but spent more of it with the Oakland Raiders, also made the list). In 2005, TSN published another special feature honoring the 50 Greatest Quarterbacks. Elway was ranked third behind Johnny Unitas and Joe Montana.

Elway was co-owner of the Arena Football team Colorado Crush, from their inception in 2002 until the cancellation of the Arena Football League after the 2008 season. In February 2007, Elway was elected chairman of the AFL’s executive committee. On August 4, 2009, the Arena Football League announced an indefinite suspension of operations. Elway was one of the 17 remaining franchise owners that voted to suspend operations indefinitely.

On August 8, 2004, Elway was inducted into the Pro Football Hall of Fame. He was elected in his first year of eligibility. He was presented by his eldest daughter Jessica. He was inducted into the College Football Hall of Fame in 2000.

Elway met former Oakland Raiders cheerleader Paige Green in 2005 at a celebrity golf tournament held by former Raiders running back Marcus Allen in Los Angeles. They were engaged in Italy in September 2008, and married in August 2009.

In September 2008, Elway became the spokesperson for OpenSports.com.

Elway had LASIK eye surgery and endorsed Icon LASIK in the Denver area in November 2008.

In December 2010, Elway expressed interest in working as the Broncos’ top football executive, after having dinner with Broncos owner Pat Bowlen. However, he expressed no interest in being a head coach or general manager after Josh McDaniels’ firing, saying, “I’m not interested in being a head coach. I’m not interested in being a general manager. I don’t have that kind of experience to be able to pick those players day in and day out and such.”

On January 5, 2011, Elway was named general manager and executive vice president of football operations of the Broncos, with the final say in all football matters. In this capacity, he reports to team president Joe Ellis and is the immediate supervisor for the head coach of the team. General manager Brian Xanders was actually retained, but served mostly in an advisory role to Elway. Xanders left the team after the 2011 season, and Elway assumed the role of general manager which gave him complete control over the football side of the Broncos operation.

Elway hired Gary Kubiak, his former backup quarterback and former Broncos offensive coordinator, as the new head coach for the 2015 season. Elway and Kubiak also brought back Wade Phillips, a former Broncos head coach, for his second stint as the team’s defensive coordinator. Elway won a third Super Bowl as part of the Broncos franchise, when on February 7, 2016 Denver defeated the Carolina Panthers 24-10 in Super Bowl 50. This gave him his first Super Bowl win as Executive VP/GM, to go along with the two he won as the team’s quarterback.

Elway tested positive for COVID-19 on November 3, 2020.