Benwikere committed to San Jose State on February 2, 2010. He was part of coach Mike MacIntyre's first recruiting class at San Jose State, and Benwikere played under MacIntyre from 2010 to 2012 and Ron Caragher in 2013. As a true freshman in 2010, he played in all 13 games and made 9 starts. During his sophomore year, he played in ten games and made two starts. In 2012, Benwikere was named first-team All-WAC. He played in 13 games and started 8. Benwikere scored two defensive touchdowns off a 37-yard fumble recovery against New Mexico State and 47-yard interception return against Idaho. On November 24 against Louisiana Tech, Benwikere tied a San Jose State record with three interceptions. In San Jose State's victory over Bowling Green in the 2012 Military Bowl, Benwikere blocked a punt for a safety. In his senior season in 2013, Benwikere was named first-team All-MWC, started 11 games, and had a streak of four consecutive games with an interception. In his San Jose State career, Benwikere had 214 tackles, 3 forced fumbles, 2 fumbles recovered, 14 interceptions, and 22 passes broken up. Benwikere graduated from San Jose State with a B.A. in sociology.
Professional career
Carolina Panthers
The Carolina Panthers selected Benwikere in the fifth round of the 2014 NFL Draft. The Carolina Panthers traded a fifth and seventh round pick to the Minnesota Vikings and received a fifth round pick in order to draft Benwikere. Carolina Panthers’ General Manager Dave Gettleman noted the Panthers’ had graded Benwikere as a fourth round pick. Benwikere was the 19th cornerback drafted in 2014. .
2014 season
On May 20, 2014, the Carolina Panthers signed Benwikere to a four-year, $2.41 million contract that includes a signing bonus of $199,000. As a rookie, during the preseason, Benwikere won the starting nickel corner position on the Panther defense over veteran Charles Godfrey. On his NFL debut on September 7, 2014 in Carolina's 20-14 win over the Tampa Bay Buccaneers, Benwikere had 4 tackles, 1 pass deflection, and a recovery of a forced fumble by teammate Luke Kuechly on Tampa running back Bobby Rainey. Benwikere's fumble recovery enabled Carolina to run out the clock en route to their victory. In a week 2 victory over the Detroit Lions, Benwikere allowed only 20% of his targets to catch a pass, had a pressure, and recorded a pass deflection that was nearly picked off by teammate, Star Lotulelei. Through the first two weeks of the season, Pro Football Focus rated Benwikere as the second best cornerback in the NFL, allowing a completion percentage of only 44.4% of passes thrown in his area. In the first half of the October 5 game against the Chicago Bears, Benwikere left the game in the first half after twisting his ankle. As of November 9, Benwikere has been inactive. In the Panthers week 14 game against the New Orleans Saints, Benwikere recorded his first NFL interception against Saints quarterback Drew Brees. Despite giving up 8 catches on 10 targets against the Saints, he only gave up 48 yards and his rating when targeted was a 47.1. Benwikere didn't allow a single touchdown in 254 snaps and 45 targets. On December 23, 2014, Benwikere was named to the Sports Illustrated 2014 All-Rookie Team. Over the final eight weeks of the regular season, Pro Football Focus rated Benwikere as the best cover corner in the NFL. During the Panthers playoff victory over the Arizona Cardinals, Benwikere gave up only one reception for 21 yards for the game. On January 13, 2015, Benwikere was named to the ProFootball Focus 2014 All-Rookie Team. He was also named to the All-Rookie teams for both ESPN and Sports Illustrated. For his rookie season, Benwikere allowed a rookie-low 72.9 opposing quarterback rating, no touchdowns, and was the third best in the NFL in the yards per reception allowed in 459 regular-season snaps.
2015 season
With the Panthers acquisition of Charles Tillman during the offseason, Benwikere was named the Panthers starting nickelback to open the season. Through the first three weeks of the season, the only two cornerbacks who were targeted 20 or more times and had not allowed a pass for more than 16 yards were Benwikere and teammate, Josh Norman. During the Panthers 44-16 victory over the Washington Redskins, Benwikere recorded his first career strip-sack against quarterback Kirk Cousins and only allowed 14 receiving yards in his zone. On December 13, during a game against the Atlanta Falcons, Benwikere suffered a fractured leg, and was placed on season-ending injury reserve. On February 7, 2016, Benwikere's Panthers played in Super Bowl 50. In the game, the Panthers fell to the Denver Broncos by a score of 24–10.
2016 season
On October 7, Benwikere was released by Carolina after the Panthers defense allowed 300 receiving yards to Atlanta Falcons' wide receiver Julio Jones for only the sixth such occurrence in NFL history. Benwikere admitted having some "conditioning issues", allowing the Falcons' Jones to get a step on him.
Benwikere was claimed off waivers by the Miami Dolphins on October 10, 2016. He was released by the Dolphins on November 8, and was re-signed to the practice squad.
On September 2, 2017 the Dallas Cowboys traded a conditional 2019 sixth-round draft pick to the Cincinnati Bengals in exchange for Benwikere. The Cowboys acquired him to provide depth while rookies Chidobe Awuzie and Jourdan Lewis recovered from hamstring strains. He appeared in 12 games playing mainly on special teams, registering 2 tackles in only 10 defensive snaps.
Arizona Cardinals
On March 23, 2018, Benwikere signed with the Arizona Cardinals, reuniting with head coachSteve Wilks who was his defensive backs coach with the Panthers. He played in 11 games, starting eight, before being released by the Cardinals on November 26, 2018.