The history of the Buffalo Bills began in October of 1959, though their first game was in 1960, when the team began play as a charter member of the American Football League (AFL), winning two consecutive AFL titles in 1964 and 1965. The club joined the National Football League (NFL) as part of the 1970 AFL-NFL merger. The Bills have the distinction of being the only team to advance to four consecutive Super Bowls between 1990 and 1993, but also the regrettable distinction of losing all four of them.

The second NFL team to represent Buffalo, New York, the Bills were founded by Ralph Wilson, who owned the team from its establishment until his death in 2014. Wilson's estate sold the team to Terrence Pegula and his wife Kim later that year.

Professional football in Buffalo before 1960

The Bills were not the first professional football team to play in Buffalo, nor was it the first NFL team in the region. Professional football had been played in Buffalo and in western New York since the beginning of the 20th century. In 1915, Barney Lepper's "Buffalo All-Stars" were founded; the team would later be replaced by the Niagaras in 1918, then the Prospects in 1919. The Prospects were the basis of what would become the "Buffalo All-Americans," who joined what would become the NFL in 1920. After changing their name to the Bisons in 1924 (and, for one season, the Rangers in 1926), the team suspended operations in 1927, then came back in 1929 and re-folded at the end of that season.

After Buffalo hosted two NFL games in 1938 (a practice that would become a semi-regular occurrence in the city until the current team's arrival), the third American Football League installed the Buffalo Indians in the city; the Indians played two years before the league suspended and ultimately folded due to World War II. After the war, when the All-America Football Conference formed, Buffalo was again selected for a team; originally known as the Buffalo Bisons, the same name as a baseball team and (at the time) a hockey team in the area, the team sought a new identity and named itself the "Buffalo Bills" in 1947. When the AAFC merged with the NFL in 1950, the AAFC Bills were merged into the Cleveland Browns. Though there was no connection between the AAFC team and the current team, the Bills name proved popular enough that it was used as the namesake for the future American Football League team that would form in 1959.

The forerunners to the Canadian Football League would also play at least one game in Buffalo in 1951. For a period in the 1950s, Silas Rooney hosted the Pittsburgh Steelers training camps at Forness Stadium on the campus of St. Bonaventure University, which allowed the team to play an annual exhibition in Buffalo and/or Rochester.

1960–1985 Bringing pro football back to Buffalo

When Lamar Hunt announced the formation of the American Football League in the summer of 1959, Buffalo was one of the target cities Hunt sought. His first choice of owner, however, turned him down; Pat McGroder (then a liquor store owner and sports liaison with the city of Buffalo) was still hopeful that the threat of the AFL would prompt the NFL to come back to Buffalo to try to stop the AFL from gaining a foothold there (as the NFL would do with teams in Minnesota, Dallas, St. Louis and later Atlanta). McGroder's hopes never came to fruition.

Harry Wismer, who was to own the Titans of New York franchise, reached out to Detroit insurance salesman and automobile heir Ralph C. Wilson Jr. to see if he was interested in joining the upstart league. (Both Wismer and Wilson were minority owners of NFL franchises at the time: Wilson held a stake in the Detroit Lions, while Wismer was a small partner in the Washington Redskins but had little power due to majority owner George Preston Marshall's near-iron fist over the team and the league). Wilson agreed to field a team in the new league, with the words "Count me in. I'll take a franchise anywhere you suggest."

Hunt gave Wilson the choice of six cities: Miami, Buffalo, Cincinnati, St. Louis, Atlanta, or Louisville, Kentucky. Wilson's first choice was Miami, but local officials there were wary of an upstart league after the failure of the All-America Football Conference's Miami Seahawks over a decade prior. They refused to let an AFL team play at the Orange Bowl, and the city had no other venue suitable for even temporary use. Wilson reached out to an acquaintance from his military days in World War II who lived in Buffalo: general contractor George E. Schaaf. Schaaf assured Wilson that pro-football interest was significant in Buffalo and assembled a coalition of key Buffalo figures, including Pat McGroder (a mutual friend of both), who were able to interest Wilson in bringing the AFL franchise to Buffalo. Attorney Paul Crotty (father of Paul A. Crotty and a powerful Buffalo political figure) and McGroder negotiated a sweetheart deal with Civic Stadium in Buffalo—which at the time was primarily an auto racing track but was the only venue with enough seating to accommodate a team (since Offermann Stadium, the city's baseball park and the home of the city's 1920s NFL teams, was undersized, surrounded by residential housing where owners had erected its own rooftop stands allowing spectators to watch the game without paying admission to the teams that played there, and had been condemned by city code enforcement)—and offered Wilson full control of the venue and a deep discount on rent. Wilson promptly removed the racetrack and had Civic Stadium transformed into War Memorial Stadium, which would house both baseball and football. Wilson sent Hunt a telegram with the now-famous words, "Count me in with Buffalo."Buffalo News 10/17/59 – Buffalo News 10/24/59 – Buffalo Bills Media Guide, 1960 – NY Journal 8/22/60 – Buffalo Bills Media Guide 1964.

Most of Wilson's other choices would receive their own professional football franchises during the AFL's ten-year run. Before the AFL had even played a game, the NFL had responded by moving the moribund Chicago Cardinals to St. Louis, where they would share their nickname with the long-established baseball team. After the AFL established itself, Miami reversed its stance and granted the Miami Dolphins a lease for the city-owned Orange Bowl, where they commenced play in 1966. Meanwhile, the Atlanta Falcons would join the NFL in 1967, while the Cincinnati Bengals would become the AFL's tenth (and final) team in 1968. On the other hand, Louisville has yet to be home to a team in any of the established U.S. major professional sports leagues and would not receive a fully professional football team until the Louisville Kings were established in 2026.

1960–1963: The early AFL years

The Buffalo Bills were a charter member of the American Football League (AFL) in 1960. After a public contest, the team adopted the same name as the AAFC Buffalo Bills, the former All-America Football Conference team in Buffalo. The AAFC Bills franchise was named after the Buffalo Bills, a popular barbershop quartet, whose name was a play on the name of the famed Wild West showman Buffalo Bill Cody. The franchises are not officially related, other than in name, to each other.

After an inaugural season that saw the Bills finish 5–8–1 (third in the four-team AFL East Division), the Bills gained four of the first five picks in the 1961 AFL draft, including the top slot, which they used to draft offensive tackle Ken Rice. They also drafted guard Billy Shaw in the same draft. Success did not come overnight. On August 8, 1961, the Bills became the first (and only) American Football League team to play a Canadian Football League team, the nearby Hamilton Tiger-Cats. Because of that game, they also hold the dubious distinction of being the only current NFL team to have ever lost to a CFL team, as the Tiger-Cats won, 38–21. Hamilton was one of the best teams in the CFL (they would go on to win the Big Four title but lose in the 49th Grey Cup that year), and Buffalo, at the time, was the worst team in the AFL.

In the 1962 offseason, Buffalo stocked up on players that would play key roles in the successful years of the mid-1960s. Jack Kemp was acquired off waivers from the San Diego Chargers after the Chargers thought Kemp, who had led the Chargers to back-to-back AFL title games, had a bum hand. The Bills also drafted Syracuse running back phenomenon Ernie Davis and had a serious chance of getting him to play for Buffalo after the Redskins, a team Davis refused to play for, drafted him; however, Davis instead opted to play for the NFL after the Redskins traded him to Cleveland, and he died of leukemia before playing a single down of professional football. Instead, the Bills then acquired one of the CFL's top running backs, Cookie Gilchrist.

On December 14, 1963, the Bills and the New York Jets played the final game at the Polo Grounds.

The mid-1960s: Four straight playoffs, three division titles, back to back championships From 1963 to 1966, Buffalo experienced its first stretch of success, making the playoffs all four years and winning back-to-back AFL championships in 1964 and 1965 under head coaches Lou Saban through 1965; and Joe Collier in 1966.

The 1964 squad compiled a 12–2 regular season mark and went on to defeat the favored defending AFL champion San Diego Chargers, 20–7 at Buffalo's War Memorial Stadium on December 26, 1964. A turning point in that game occurred in the first quarter with the Chargers ahead 7–0 and driving, when Buffalo linebacker Mike Stratton broke up a flare pass to star Charger halfback Keith Lincoln with a well-timed, hard shot to the ribs, forcing Lincoln to leave the game. This is memorialized in Bills and AFL lore as the "hit heard 'round the world". Players and the fans present acknowledge that the energy in the stadium immediately changed in that instant; San Diego defensive end Earl Faison testifies of the impact it had on the game in this video

Also of note in 1964, the Bills' defense surrendered a mere 65.5 yards rushing per game and started a streak of 16 consecutive regular season games without giving up a rushing touchdown that continued well into the 1965 season (17 if the 1964 championship game is counted); this is still a professional football record as of January 2023. The Bills survived a late-season controversy when star fullback Gilchrist refused to take the field with his teammates at a critical time during a week 10 clash with the (then Boston) Patriots and coach Saban "fired" him off the team; quarterback Kemp, who would go on to the U.S. Congress and to Secretary of Housing and Urban Development under President George H. W. Bush, brokered a reconciliation between Gilchrist and Saban and the fullback rejoined the team days later.

In 1965, Buffalo's offense was hampered all season by injuries to its star receivers Glenn Bass and Elbert (Golden Wheels) Dubenion; additionally, league-leading rusher Gilchrist had been traded to the Denver Broncos. The Bills adjusted, riding their stellar defense and a short, controlled passing game to a 10–3–1 record and a second consecutive AFL Eastern Division title. The team's offensive unit received significant contributions from newly acquired Bills Bo Roberson, Jack Spikes and Billy Joe en route to a championship game rematch with the Chargers, who had smashed Buffalo 34–3 earlier in the season and again were heavily favored. This time, the Bills shut out San Diego's high-powered offense 23–0 on the Chargers' home field, Balboa Stadium. Buffalo cornerback Butch Byrd electrified Bills fans with a 74-yard punt return for a touchdown, and the defense registered five sacks on San Diego's dangerous quarterback, John Hadl.