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Professional era

On November 12, 1892, Pudge Heffelfinger was paid $500 (equivalent to $16,956 in 2023) to play a game for the Allegheny Athletic Association against the Pittsburgh Athletic Club. This is the first recorded instance of a player being paid to participate in a game of American football, although many athletic clubs in the 1880s offered indirect benefits, such as helping players attain employment, giving out trophies or watches that players could pawn for money, or paying double in expense money. Despite these extra benefits, the game had a strict sense of amateurism at the time, and direct payment to players was frowned upon, if not prohibited outright.

Over time, professional play became increasingly common, and with it came rising salaries and unpredictable player movement, as well as the illegal payment of college players who were still in school. The National Football League (NFL), a group of professional teams that was originally established in 1920 as the American Professional Football Association, aimed to solve these problems. This new league's stated goals included an end to bidding wars over players, prevention of the use of college players, and abolition of the practice of paying players to leave another team. By 1922, the NFL had established itself as America's premier professional football league.

The dominant form of football at the time was played at the collegiate level. The upstart NFL received a boost to its legitimacy in 1925, however, when an NFL team, the Pottsville Maroons, defeated a team of Notre Dame all-stars in an exhibition game. A greater emphasis on the passing game helped professional football to distinguish itself further from the college game during the late 1930s. Football, in general, became increasingly popular following the 1958 NFL Championship game between the Baltimore Colts and the New York Giants, still referred to as the "Greatest Game Ever Played". The game, a 23–17 overtime victory by the Colts, was seen by millions of television viewers and had a major influence on the popularity of the sport. This, along with the innovations introduced by the new American Football League (AFL) in the early 1960s, helped football to become the most popular sport in the United States by the mid-1960s.

The rival AFL arose in 1960 and challenged the NFL's dominance. The AFL began in relative obscurity but eventually thrived, with an initial television contract with the ABC television network. The AFL's existence forced the conservative NFL to expand to Dallas and Minnesota in an attempt to destroy the new league. Meanwhile, the AFL introduced many new features to professional football in the United States: official time was kept on a scoreboard clock rather than on a watch in the referee's pocket, as the NFL did; optional two-point conversions by pass or run after touchdowns; names on the jerseys of players; and several others, including expansion of the role of minority players, actively recruited by the league in contrast to the NFL. The AFL also signed several star college players who had also been drafted by NFL teams. Competition for players heated up in 1965, when the AFL New York Jets signed rookie Joe Namath to a then-record $437,000 contract (equivalent to $ 4.23 million in 2023). A five-year, $40 million NBC television contract followed, which helped to sustain the young league. The bidding war for players ended in 1966 when NFL owners approached the AFL regarding a merger, and the two leagues agreed on one that took full effect in 1970. This agreement provided for a common draft that would take place each year, and it instituted an annual World Championship game to be played between the champions of each league. This championship game began play at the end of the 1966 season. Once the merger was completed, it was no longer a championship game between two leagues and reverted to the NFL championship game, which came to be known as the Super Bowl.

College football maintained a tradition of postseason bowl games. Each bowl game was associated with a particular conference and earning a spot in a bowl game was the reward for winning a conference. This arrangement was profitable, but it tended to prevent the two top-ranked teams from meeting in a true national championship game, as they would normally be committed to the bowl games of their respective conferences. Several systems have been used since 1992 to determine a national champion of college football. The first was the Bowl Coalition, in place from 1992 to 1994. This was replaced in 1995 by the Bowl Alliance, which gave way to the Bowl Championship Series (BCS) in 1997. The BCS arrangement proved to be controversial, and was replaced in 2014 by the College Football Playoff (CFP).