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On March 18, 2020, Rush re-signed with the Cowboys on a one-year restricted free agent tender. On May 4, Rush was waived by the Cowboys after the team signed former Cincinnati Bengals quarterback Andy Dalton.

Rush was claimed off waivers by the New York Giants on May 5, 2020. He was reunited with his head coach from his tenure with the Dallas Cowboys, Jason Garrett, who was hired as the Giants offensive coordinator during the off-season.

As a senior he received All-State, Associated Press’ Michigan Division 5/6 Player of the Year and ESPN’s Michigan Gatorade Player of the Year honors.

In his redshirt season, he was named the school’s Scout Team Player of the Year. As a freshman, although he began the season as the third-string quarterback, he was named the starter by the third game, after Cody Kater was injured (collarbone fracture) and his backup Alex Niznak couldn't move the offense against the University of New Hampshire. In that contest he came in the second quarter and helped engineer a 24–21 come from behind victory, where he tallied 326 passing yards and 3 touchdowns, tying the school record for the longest in history (97 yards). He would never relinquish the position or miss a start after the game.

On May 12, 2017, the Dallas Cowboys signed Rush as an undrafted rookie free agent.

Coming out of Central Michigan, Rush was projected by the majority of NFL draft experts and analysts to be a seventh round pick or a priority undrafted free agent. On December 6, 2016, it was announced that Rush had accepted his invitation to the East–West Shrine Game. On January 21, 2017, Rush performed in the East–West Shrine Game for the East and completed 11 of 17 pass attempts for 97-yards in a 3–10 loss to the West. He received an invitation to the NFL combine and performed almost all of the required drills except for the bench press. He had an underwhelming lackluster performance and had some of the lowest marks at the combine. On March 20, 2017, Rush participated at Central Michigan's pro day and chose to attempt the vertical jump, broad jump, short shuttle, and three-cone drill once again. He gave a slower time in the three-cone drill (7.28), but was able to have better results in the vertical (30"), broad (8'11"), and short shuttle (4.46). He was among ten players from CMU, Northern Michigan, and Ferris State to perform combine and positional drills for scouts and team representatives from the NFL. Rush was ranked the 14th best quarterback prospect in the draft by NFLDraftScout.com.

His best season came as a junior in 2015, through the first 13 games he had 3,703 passing yards, which was a new school single-season record. He completed 66.3 percent of his passes for 3,848 total passing yards, 25 touchdowns, and 11 interceptions.

As a sophomore, he played in the 2014 Bahamas Bowl against Western Kentucky. By the middle of the third quarter, his team had fallen behind 49–14, but scored 4 unanswered touchdowns and were down by only 7 points near the end of the fourth quarter. With one second remaining on the contest, Central Michigan had the ball on their own 25 yard line. The would be final play started with a 45-yard Hail Mary pass from Rush to wide receiver Jesse Kroll. As Kroll was being tackled he lateraled the ball to teammate Deon Butler, who ran 20 yards before lateraling to Courtney Williams. With no space to run, Williams made a quick third lateral pass to leading receiver Titus Davis who ran the final 13 yards, scoring a touchdown that would have tied the game with a kicked extra point and sent the game into overtime, but instead Central Michigan attempted a two-point conversion for the win, which was unsuccessful. Had the try succeeded, it would have marked the largest comeback in bowl history and tied the largest comeback in any Division I game. His seven touchdown passes set an all-time record for all bowl games.

As a senior, his production dropped to 3,540 passing yards, 23 touchdowns, but with 16 interceptions and a low 59.8 completion percentage. Against Oklahoma State University, the game sparked controversy after the officials made an incorrect call that would eventually give Central Michigan the win. Oklahoma State threw the ball away to end the game and received a penalty for intentional grounding. Under college football rules, the game would have ended and Oklahoma State would have won the game. However, the officials gave Central Michigan an untimed down, and Rush threw a 51-yard Hail Mary pass to wide receiver Jesse Kroll, who made a lateral to fellow receiver Corey Willis at the 12-yard line, running for a touchdown with no time remaining for a 30–27 win. The team lost 10–55 in the 2016 Miami Beach Bowl at the end of the season.

Following multiple productive preseason performances in the Hall of Fame Game and the next two contests, he began to share second-team reps in practice with backup quarterback Kellen Moore before the preseason game against the Oakland Raiders. During the contest, he was given most of the time with the second-team offense and completed 12 of his 13 attempts for 115-yards and two touchdowns in a comeback 24–20 victory. He finished the preseason with a total of 38 pass completions out of 51 attempts, 398 passing yards, and six touchdown passes with no interceptions. Head coach Jason Garrett named Rush the Cowboys' third quarterback on their depth chart, behind Dak Prescott and Moore. Rush did not dress for the first five games and was a healthy scratch. Rush was promoted to second string for the sixth game of the season. Moore was then released and signed to the Cowboy's practice squad. In Week 7, in the 40–10 victory over the San Francisco 49ers, he appeared late in the game in relief of Prescott. He was 1-of-3 passing for 2 yards and had 2 rushes for 13 yards in his NFL debut.

In 2010 and 2011, he led his team to back-to-back undefeated regular seasons. In 2011, he led his team to the state runner-up title. In the Division 5 regional championship game against Dowagiac Union High School, he set Michigan state records with 5 touchdown passes in one quarter and 8 for the game. The team would end up losing in the finals against Powers Catholic High School 26–56, even though he registered 300 passing yards and 3 touchdowns.

Cooper Rush (born November 21, 1993) is an American football quarterback for the New York Giants of the National Football League (NFL). He played college football at Central Michigan University, and was signed by the Dallas Cowboys as an undrafted free agent in 2017.