Although the Can-Am League never operated with more than six teams, the departure of the Boston Bruin Cubs after the 1935–36 season reduced it down to just four member clubs: the Springfield Indians, Philadelphia Ramblers, Providence Reds, and New Haven Eagles for the first time in its history.

A little more than a month into that first season, the balance and symmetry of the new combined circuit suffered a setback when its membership unexpectedly fell to seven teams.

At the end of the 1936–37 season, a modified three-round playoff format was devised and a new championship trophy, the Calder Cup, was established.

The Syracuse Stars defeated the Philadelphia Ramblers in the final, three-games-to-one, to win the first-ever Calder Cup championship.

After two seasons of interlocking play, the governors of the two leagues' seven active teams met in New York City on June 28, 1938, and agreed that it was time to formally consolidate.

The new I-AHL also added an eighth franchise at the 1938 meeting to fill the void in its membership left by the loss of Buffalo two years earlier with the admission of the then two-time defending Eastern Amateur Hockey League (EAHL) champion Hershey Bears.

In the late 1960s and early 1970s, however, the cost of doing business in professional ice hockey began to rise sharply with NHL expansion and relocation (the NHL placed teams in Pittsburgh and Buffalo, forcing two long-time AHL clubs, the Pittsburgh Hornets and Buffalo Bisons, to fold) and especially the 1972 formation of the World Hockey Association (WHA), which forced the relocation and subsequent folding of the Cleveland Barons, Baltimore Clippers, and Quebec Aces.

The league bottomed out in the summer of 1977, with news that the Rhode Island (formerly Providence) Reds – the last remaining uninterrupted franchise from the 1936–37 season, and the oldest continuously operating minor league franchise in North America – had decided to cease operations after 51 years in Rhode Island.

The folding of the NAHL, meanwhile, suddenly left two of its stronger teams, the Philadelphia Firebirds and Binghamton, New York-based Broome Dusters, without a league to play in.

With franchise stability improving after the demise of the WHA in 1979, the league continued to grow steadily over the years, reaching 20 clubs by the 2000–01 season.

In 2001–02, the AHL's membership jumped dramatically to 27 teams, mostly by the absorption of six teams—Milwaukee, Chicago, Houston, Utah, Manitoba, and Grand Rapids—from the International Hockey League.

The IHL had established itself as the second top-level minor league circuit in North America, but folded in 2001 due to financial problems.

The Chicago Wolves (2002, 2008, 2022), Houston Aeros (2003), Milwaukee Admirals (2004), and Grand Rapids Griffins (2013, 2017) have all won Calder Cup titles since joining the AHL from the IHL.

This left Chicago, Grand Rapids and Milwaukee as the only ex-IHL teams still in their original cities until the 2015 relocations when the IceCaps moved back to Winnipeg as the Manitoba Moose.

Beginning with the 2015–16 season, twelve franchises have since relocated due to NHL parent clubs' influence on their development teams and players.

In 2016, the Springfield Falcons franchise was purchased by the Arizona Coyotes and relocated to become the Tucson Roadrunners and join the one-year-old Pacific Division.

The Falcons were subsequently replaced by the Springfield Thunderbirds, the relocated Portland Pirates franchise under a new ownership group.

[19] However, the Hurricanes loaned some players to the Wolves, such as Vasili Ponomaryov, Domenick Fensore, Ronan Seeley and Antti Raanta.

These six annual games pitted a team of all-stars against the defending Calder Cup champions (with the exception of the 1959-60 event, which featured the Springfield Indians).

On January 6, 2012, the largest crowd in AHL history saw the Adirondack Phantoms defeat the Hershey Bears, 4–3, in overtime before 45,653 fans at Citizens Bank Park in Philadelphia, as the final event of the week-long activities associated with the 2012 NHL Winter Classic, which also included a game between the Philadelphia Flyers and the New York Rangers on Jan 2 and an alumni game between retired players (including eight honored members of the Hockey Hall of Fame) of those two clubs on December 31, 2011.

The contest was the third outdoor game in AHL history and it more than doubled the league's previous single-game attendance mark.

A year after their originally scheduled date, the Griffins and Marlies played at Comerica Park on December 30, 2013, and Toronto prevailed in a shootout, 4–3, becoming the first AHL team ever with two outdoor wins.

On December 18, 2015, the Stockton Heat defeated the Bakersfield Condors, 3–2, at Raley Field in West Sacramento, California.

Prior to the 1980 Winter Olympics in Lake Placid, New York, the Adirondack Red Wings hosted exhibition games against the national teams from the United States, West Germany, Sweden and Finland.

[32] In 2014, Swedish club Färjestad BK met the Toronto Marlies as part of a visit to Canada that included its participation in the 2014 AHL All-Star Classic.

[33] In February 2018, the Ontario Reign hosted and defeated the DEL's Eisbären Berlin, 6–3, in a friendly matchup organized by Anschutz Entertainment Group, the owner of both teams.