A new era for the Winnipeg Arena began in the fall of 1972 when the city's new professional hockey team, the Winnipeg Jets, entered the upstart WHA. Their on-ice success during the 1970s brought three WHA championship banners to the rafters of the arena and made the Jets the pride of the city and province.

In 1979, the Jets were one of four teams admitted into the National Hockey League following the demise of the WHA, which necessitated a major expansion to the arena. The seating capacity was expanded to 15,565, mostly through the construction of upper decks on the east and west sides. The construction of these upper decks created an overhang above the lower deck seating areas, obstructing views according to many spectators. That same year, a painting of Queen Elizabeth II was commissioned for the arena by Francis Lawrence Jobin, the Lieutenant Governor of Manitoba. The painting measured 5 by 7 metres (16 by 23 ft) (one of the largest ever painted of the Queen) and hung from the arena's rafters. A White Way sign centre-hung scoreboard with colour matrix animation boards replaced an American Sign and Indicator centre-hung scoreboard circa 1987. The American Sign and Indicator scoreboard, in use since the 1980–1981 season, was moved to Copps Coliseum in Hamilton, Ontario.

During the 1980s, a tradition known as the "White Out" was initiated in which boisterous and sometimes raucous fans dressed in all-white during playoff games to create an intimidating environment for opposing teams. This led to the Winnipeg Arena's reputation as one of the loudest sports venues in North America during the 1980s and 1990s. This tradition continued with the revived Jets team in 2011.

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