At William Howard Taft High School, Dinwiddie was recognized as one of the greatest standout athletes since Jordan Farmar.

[1] In the first regular season game for Colorado, Dinwiddie made his collegiate debut in a 32-point victory over Fort Lewis with seven points and seven rebounds.

The departures of Carlon Brown and Nate Tomlinson were instrumental in Dinwiddie's breakout sophomore season, when he earned first-team All-Pac-12 honors.

The Buffaloes won the 2012 Charleston Classic, in which Dinwiddie took the role as starting small forward in the final three rounds.

[9] Dinwiddie continued to act as the leader of the Colorado Buffaloes men's basketball team through the beginning of his junior year.

He helped the team win 14 of their first 16 regular season games, which made them one of the most successful underdogs in the country, most notably toppling the Kansas Jayhawks due to a game-winner from Askia Booker.

Dinwiddie reportedly made contact with Russ Paine, who helped Adrian Peterson recover from his ACL injury and become the 2012 NFL MVP.

[19][20] However, after struggling in the next four games, he fell out of the rotation, compounded by Blake's form improvement and Brandon Jennings returning from injury.

[19] Dinwiddie played a season-high 29 minutes in the Pistons' regular-season finale on April 13, scoring 12 points in a 112–110 overtime win over the Cleveland Cavaliers.

[26] He then spent the start of the 2016–17 season with Chicago's D-League affiliate team, the Windy City Bulls,[27] averaging 19.4 points, 8.1 assists and 3.7 rebounds over 37.4 minutes in nine games.

[29] On April 8, 2017, in a 107–106 win over the Chicago Bulls, Dinwiddie made four free throws in the final 13.6 seconds and finished with 19 points.

[30] On October 25, 2017, Dinwiddie scored a career-high 22 points and hit the go-ahead 3-pointer with 43 seconds left to lift the Nets to a 112–107 win over the Cleveland Cavaliers.

[35] On January 3, 2018, he made the go-ahead jumper with 10.1 seconds left and tied his career high with 26 points, leading Brooklyn to a 98–97 victory over the Minnesota Timberwolves.

[47] Two days later, it was revealed that a right thumb injury that he had originally hurt roughly two months earlier and had gotten progressively worse would require surgery, having suffered torn ligaments.

[50] With 28 points against the Cavaliers on March 6, Dinwiddie had his 14th 20-point game off the bench to set a Nets single-season record—Darryl Dawkins, Purvis Short and Orlando Woolridge all had 13.

[53] On January 28, 2020, Dinwiddie switched his jersey number from 8 to 26 after the approval of the NBA, in honor of the late Kobe Bryant.

[55] On December 27, 2020, Dinwiddie left a game between the Nets and the Charlotte Hornets with a suspected right knee strain,[56] which was later revealed to be a season-ending partial ACL tear.

[57][58] On August 6, 2021, Dinwiddie was acquired by the Washington Wizards via a sign-and-trade deal involving five teams, sending Russell Westbrook to the Los Angeles Lakers.

[59] He made his Wizards debut on October 20, logging 13 points, four rebounds and six assists in a 98–83 win over the Toronto Raptors.

[60] On October 22, Dinwiddie scored 34 points, alongside six rebounds and nine assists, in a 135–134 overtime win over the Indiana Pacers.

[61] On February 10, 2022, Dinwiddie was traded, along with Dāvis Bertāns, to the Dallas Mavericks in exchange for Kristaps Porziņģis and a protected 2022 second-round pick.

[73] On March 24, 2024, Dinwiddie scored a team high 26 points, alongside two rebounds and five assists, in a 150–145 win against the Indiana Pacers.

[75] In 2013, Dinwiddie was named to the USA Basketball Men's World University Games Team for the 2013 Summer Universiade in Kazan, Russia.

He averaged 7.9 points and 2.6 rebounds per game and led Team USA with 44 assists (5.5 apg) and with 12 steals (1.5 spg).