He played college football for the Baylor Bears and was selected in the second round of the 2016 NFL draft by the Miami Dolphins, where he spent eight seasons with the team.

During his tenure in Miami, Howard was a four-time Pro Bowler, a two-time All-Pro member, and led the league in interceptions twice.

He attended and played football at Wheatley High School in the city, where he was teammates with fellow NFL cornerback William Jackson III.

[10] Howard opted to redo the majority of workouts and improved on all his combine numbers with scouts and representatives from all 32 NFL teams looking on.

[22] On the final day of minicamp, Howard suffered a knee injury and was placed on the physically unable to perform list after it was discovered he would require surgery.

[23] Although he missed the first three preseason games, head coach Adam Gase elected to name Howard the second starting cornerback, alongside veteran Byron Maxwell, to begin the regular season.

[26] On December 17, 2016, Howard appeared in his first game since his knee injury and collected three solo tackles and had a season-high three pass deflections during a 34–13 victory at the New York Jets.

[31] Howard started the Dolphins' season-opener at the Los Angeles Chargers and recorded a season-high seven combined tackles during their 19–17 victory.

In Week 13, Howard recorded a solo tackle, a season-high five pass breakups, two interceptions, and returned one for a touchdown during the Dolphins' 35–9 win against the Denver Broncos.

[32] The following week, he deflected three passes and intercepted New England Patriots quarterback Tom Brady twice during their 27–20 win on Monday Night Football.

[33] On December 17, 2017, Howard collected four solo tackles and made his first career sack on Tyrod Taylor, as the Dolphins were defeated by the Buffalo Bills 24–16.

In Week 13 of the 2018 season, Howard injured his knee after intercepting Bills' quarterback Josh Allen for the second time that afternoon.

Howard ended the 2018 season leading the league interceptions with Chicago Bears corner Kyle Fuller and Atlanta Falcons safety Damontae Kazee with seven.

[51] In Week 14 against the Kansas City Chiefs, Howard recorded a one handed interception off a pass thrown by Patrick Mahomes during the 33–27 loss.

[52] In Week 17 against the Bills, Howard recorded his league leading 10th interception of the season off a pass thrown by Matt Barkley during the 56–26 loss.

[56] In July 2021, Howard announced that he had requested a trade from the Dolphins due to feeling undervalued and underpaid, also stating "I am just here so I don't get fined" in regards to him reporting to training camp.