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Smith finished the 2019 season setting career-highs in receptions with 35 and receiving yards with 439 along with tying a career-high in touchdowns with three. He also rushed four times for 78 yards.

Smith entered the 2018 season as the Titans' No. 2 tight end behind veteran Delanie Walker. He was named the top tight end on the depth chart after Walker suffered a dislocated ankle during the season-opening 27-20 road loss to the Miami Dolphins. Smith initially struggled filling Walker's shoes but he caught his first touchdown of the season on a shovel pass from Mariota during Week 9 against the Dallas Cowboys in a 28-14 road victory. In the next game against the New England Patriots, Smith caught four passes for 45 yards and a touchdown in the 34–10 victory. Two weeks later, he caught a 61-yard touchdown pass as the Titans lost to the Houston Texans on the road by a score of 34–17. However, during a 30–9 victory against the Jacksonville Jaguars in Week 14, he suffered a season-ending MCL injury.

Smith finished the 2018 season with 20 receptions for 258 yards and three touchdowns. Without Smith, the Titans finished with a 9–7 record and narrowly missed out on the playoffs.

On January 17, 2017, it was announced that Smith had accepted an invitation to play in the 2017 Senior Bowl. He practiced well during the week prior to the Senior Bowl, but was overshadowed by other tight ends who were considered first and second round picks. On January 28, 2017, Smith played in the Reese's Senior Bowl for Chicago Bears' head coach John Fox 's North team who lost 16–15 to the South. Smith was one of 19 tight ends who received an invitation to attend the NFL Scouting Combine in Indianapolis, Indiana. Smith had an impressive performance and finished in the five among tight ends in the majority of the drills. He placed second in the vertical jump and short shuttle, tied for third in the bench press, fourth in the broad jump, and finished sixth in the 40-yard dash in his position group. On March 29, 2017, Smith opted to participate at FIU's pro day, along with Dieugot Joseph and ten other teammates. He performed the three-cone drill and positional drills for scouts and team representatives from 29 NFL teams and the Winnipeg Blue Bombers of the Canadian Football League. Throughout the pre-draft process, Smith had private workouts and visits with Atlanta Falcons, Tennessee Titans, New Orleans Saints, Miami Dolphins, and Minnesota Vikings. At the conclusion of the pre-draft process, Smith was projected to be a fourth or fifth round pick by NFL draft experts and analysts. He was ranked the tenth best tight end in the draft by NFLDraftScout.com and was ranked the 12th best tight end by NFL analyst Gil Brandt.

The Tennessee Titans selected Smith in the third round (100th overall) of the 2017 NFL Draft. Smith was the sixth tight end selected in 2017 and was the seventh player selected in FIU's school history. He was the third-highest selection in school history, behind the Indianapolis Colts' wide receiver T. Y. Hilton (92nd overall, 2012) and former Jacksonville Jaguars safety Johnathan Cyprien. (33rd overall, 2013). He also became teammates with Cyprien who signed with the Tennessee Titans as a free agent during the offseason. Throughout the draft process, Smith drew numerous comparisons to the Titans' tight end Delanie Walker. The Titans selected Smith due to the heavy comparisons and to fill a void in their two tight end sets after Anthony Fasano departed in free agency. Offensive coordinator Terry Robiskie drafted Smith to complement Walker in their two tight end sets they used heavily the previous season.

On May 17, 2017, the Titans signed Smith to a four-year, $3.10 million contract that includes a signing bonus of $706,288.

Smith's best friend, Willie “Quasim” Jefferson, died from a gunshot in October 2016. Smith gave his son Jaiyen the middle name Quasim in honor of Jefferson. Smith competed in weightlifting, finishing second in the county in the 219-pound weight class.

On October 31, 2016, Smith was involved in an altercation with his girlfriend, Mary Gaspar, who was five months pregnant. The argument took place in their campus dorm room, where Gaspar used a kitchen pot and poured boiling hot water onto Smith. Smith suffered burns, and was ruled out for the rest of his senior year. Gaspar was arrested for aggravated battery, and entered a not guilty plea.

Smith credits his mother, Karen, for his successes. When Smith was four, his father passed away as a result of a tow truck accident when he went to work and was in the process of towing an abandoned car after Philadelphia mayor John Street began a campaign to rid the streets of all abandoned vehicles. The car accidentally slid off and crushed Wayne Smith, killing him at age 40. As a result, Karen raised all six children by herself. "My mother is my rock," said Smith. "It was tough, but we always got what we needed—not necessarily what we wanted all the time—but what we needed. She was so strong all the time."

Smith played college football at Florida International University. As a freshman in 2013, Smith played 12 games with 388 receiving yards and two touchdowns. As a sophomore in 2014, he played 12 games with 710 receiving yards and eight touchdowns. As a junior in 2015, he played in 8 games with 397 receiving yards and four touchdowns. As a senior in 2016, he played 11 games with 506 receiving yards and four touchdowns. Smith majored in liberal studies at Florida International.

Smith made his first NFL start and NFL debut in the Titans' season-opening 26–16 loss to the Oakland Raiders. In the next game, he recorded two receptions for 30 yards and scored his first NFL touchdown on a 32-yard screen pass from Marcus Mariota during the fourth quarter of a 37–16 road victory over the Jacksonville Jaguars. Smith had made his first NFL reception in the second quarter, losing two-yards on a short screen pass from Mariota before being tackled by linebacker Paul Posluszny. During Week 3 against the Seattle Seahawks, Smith caught a 24-yard touchdown during the third quarter of a 33–27 victory. During Week 5 against the Miami Dolphins, he caught a season-high five passes for 21 yards in the 16-10 road loss.

The Titans finished second in the AFC South with a 9–7 record and made the playoffs as a Wild Card team. In the Wild Card Round, the Titans played the Kansas City Chiefs. Smith started alongside Delanie Walker and finished the game catching two passes for 15 yards. In the Divisional Round against the New England Patriots, against the New England Patriots, Smith recorded a four-yard reception before suffering a torn MCL in the 35–14 loss.

Smith returned from his injury in time for the Titans' season opener against the Cleveland Browns. He recorded one reception for seven yards and a 10-yard rush in the 43–13 road victory. During Week 5 against the Buffalo Bills, Smith caught a 57-yard reception as the Titans lost 14–7. Two weeks later against the Los Angeles Chargers, he caught three passes for 64 yards as the Titans won 23–20. In the next game against the Tampa Bay Buccaneers, he caught six passes for 78 yards and his first touchdown of the season from Ryan Tannehill. During Week 14 against the Oakland Raiders, Smith caught three passes for 29 yards and a touchdown in the 42-21 road victory. In the next game against the Houston Texans, he caught five passes for 60 yards and had a 57-yard rush in the 24–21 loss. Smith continued his momentum the next game against the New Orleans Saints, catching three passes for 63 yards and a touchdown as the Titans lost 38–28.

The Titans finished second in the AFC South with a 9–7 record and made the playoffs as a Wild Card team. In the Divisional Round against the Baltimore Ravens, Smith caught a one-handed touchdown during the first quarter of the 28-12 road victory.

Jonnu Andre Smith (born August 22, 1995) is an American football tight end for the Tennessee Titans of the National Football League (NFL). He played college football at Florida International University.