Raymond Emmett Berry Jr. was born in Corpus Christi, Texas, on February 27, 1933, and spent the majority of his childhood in Paris, Texas. At Paris High School and in college, Berry caught very few passes. He did not start on his high school team until he was a senior, even though his father, Berry Sr., was the coach. After high school Berry played one year of junior college football at Shreiner Institute (now Schreiner University) in Kerrville, Texas, during the 1950 campaign. He helped the Mountaineers finish its most successful season in 10 years with a record of 7–3. He then transferred to Southern Methodist University (SMU). In three seasons for the SMU Mustangs football team, Berry received only 33 passes total. Sportswriters attributed his lack of receptions to his poor eyesight, but during the early 1950s, colleges specialized in the running game. As Berry said, "I didn't catch many passes because not many were thrown". He also played outside linebacker and defensive end for the Mustangs, despite weighing only 180 pounds (82 kg) even by his senior year.

Berry was drafted by the Baltimore Colts in the 20th round as the 203rd overall pick of the 1954 NFL draft. Considered a long-shot to make the team roster, he was used sparingly as a rookie, catching only 13 passes. By his second NFL season he became a permanent starter when the Colts acquired quarterback Johnny Unitas. Over the next 12 seasons together the two became one of the most dominant passing and catching duos in NFL history. Berry, who did not miss a single game until his eighth year in the league, led the NFL in receptions and receiving yards three times and in receiving touchdowns twice.

In 1957, Berry caught 47 passes for 800 yards and six touchdowns, leading the NFL in receiving yards for the first time. Against the Washington Redskins that year in near-freezing weather, Unitas connected with Berry on 12 passes for 224 yards and two touchdowns, staging what the Pittsburgh Post-Gazette called a "spectacular show". He was recognized as a first-team All-Pro by The Sporting News and earned second-team honors from the Associated Press (AP). The following season, he recorded 794 receiving yards and led the league with 56 receptions and nine touchdowns. For his efforts, Berry was invited to his first Pro Bowl, and was a first-team All-Pro by the AP and several other major selectors. The Colts finished atop the Western Division with a record of 9–3 and faced the New York Giants in the NFL Championship Game.

One of Berry's most notable performances was in that 1958 NFL Championship Game, known as "The Greatest Game Ever Played", in which he led the Colts to the franchise's first title with a then championship record 12 catches for 178 yards and a touchdown in the Colts' 23–17 victory over the Giants. At the end of regulation, he caught three consecutive passes for 62 yards to set up the Colts' tying field goal. He also had two key receptions for 33 yards during the Colts' final game-winning drive in overtime. His 12 receptions would remain an NFL championship game record for more than half a century, topped by one by Demaryius Thomas in Super Bowl XLVIII after the 2013 season.

Berry led the NFL in receptions, receiving yards, and receiving touchdowns in 1959, becoming the fourth player to record a "triple crown" in receiving. His 14 receiving touchdowns set a Colts single-season franchise record that stood unmatched for over four decades. He was invited to his second straight Pro Bowl, and earned first-team All-Pro honors from the AP, UPI, the Newspaper Enterprise Association, and the New York Daily News. The Colts won back-to-back championships in an encore with the Giants, 31–16. In that game, Berry caught five passes for 68 yards, second on the team behind halfback Lenny Moore's 126 yards on three receptions.

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After retiring from playing, Berry joined Tom Landry's Dallas Cowboys coaching staff as receivers coach. In 1970, after two seasons, Berry took a job with Frank Broyles at the University of Arkansas as receivers coach. In 1973 Berry joined Don McCafferty with the Detroit Lions as his receivers coach. In 1976, Berry joined former SMU teammate Forrest Gregg as his receivers coach with the Cleveland Browns. Berry joined the New England Patriots as receivers coach under Chuck Fairbanks in 1978. He stayed on with new coach Ron Erhardt until Erhardt and his entire staff were fired following a 2–14 1981 season. Berry left football and worked in real estate in Medfield, Massachusetts, until the Patriots fired Ron Meyer in the middle of the 1984 season and hired Berry to replace him. Under his leadership, the Patriots won four of their last eight games and finished the season with a 9–7 record. Berry's importance to the team was reflected less in his initial win–loss record than in the respect he immediately earned in the locker room – according to running back Tony Collins, "Raymond Berry earned more respect in one day than Ron Meyer earned in three years".

In the 1985 season, the team improved further, posting an 11–5 record and making the playoffs as a wild card team. They went on to become the first team in NFL history to advance to the Super Bowl by winning three playoff games on the road, defeating the New York Jets 26–14 (the second postseason win in franchise history), the Los Angeles Raiders 27–20, and the Miami Dolphins 31–14. It was the first time the Patriots had beaten the Dolphins at the Orange Bowl (Miami's then-home stadium) since 1966, Miami's first season as a franchise. The Patriots had lost to the Dolphins there 18 consecutive times, including a 30–27 loss in Week 15 of the regular season. Despite their success in the playoffs, the Patriots were heavy underdogs to the Chicago Bears in Super Bowl XX. They lost 46–10 in what was at the time the most lopsided defeat in Super Bowl history. "We couldn't protect the quarterback, and that was my fault. I couldn't come up with a system to handle the Bears' pass rush", Berry acknowledged.

The following season, Berry's Patriots again recorded an 11–5 record and made the playoffs, this time after winning their second division title as an NFL team. However, they lost in the first round of the postseason. It would be Berry's last postseason appearance in New England, and the Patriots' last playoff berth altogether until 1994. They narrowly missed the playoffs with an 8–7 record in 1987 (a strike-shortened season) and a 9–7 record in 1988, in which quarterback Doug Flutie went 6–3 as a starter. However, Berry benched Flutie in the season finale against the Denver Broncos until the final seconds. The Patriots lost 21–10 and Flutie left for the CFL less than two years later. Then in Berry's last year as a coach, the Patriots finished the 1989 season 5–11. New Patriots majority owner Victor Kiam demanded Berry relinquish control over personnel and reorganize his staff; Berry refused and was fired. His regular-season coaching record was 48–39 (.552) and he was 3–2 (.600) in the playoffs.

After a year out of coaching, Berry joined Wayne Fontes' staff with the Detroit Lions in 1991 as their quarterbacks coach, and then held the same position the following season on Dan Reeves' staff with the Denver Broncos. Reeves was fired after that season, along with his entire coaching staff.

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