Kiszkan returned to Prince Albert in 1944 to play junior hockey there. In 1945, he turned professional in the American Hockey League (AHL), where he spent eleven seasons playing mostly for the Cleveland Barons in the late 1940s and 1950s.

In the 1958 Inter-League draft he was claimed by the Toronto Maple Leafs. Nonetheless, Bower preferred to stay with the Barons, as he was tired of moving all over the country. Punch Imlach, whom the Maple Leafs had recently hired, visited Bower and convinced him to give the NHL one more try, as he considered him “the most remarkable — and maybe the best — athlete in the world.” The Leafs at this time were an up-and-coming team of young star players, and after Imlach traded for Red Kelly, the Leafs were ready for contention.

Bower won his first Vezina Trophy in 1961 for allowing the fewest goals in the 1960–61 season. The height of his NHL career came during the Maple Leafs’ three consecutive Stanley Cup victories from 1962 to 1964. He later said, “When we won the Stanley Cup, my head went numb, my whole body went numb. That was my dream from Day One. You just can’t explain the feelings inside you.”

Bower’s career was hampered by poor eyesight, but he remained a top-tier goaltender. He was known for his hard-nosed, scrappy playing style and helped the Leafs win another Stanley Cup in 1967, as part of a tandem with another Hall of Famer, Terry Sawchuk. He said, “I wasn’t all that glad to see the two-goalie system come in. I wanted to play as many games as I could.” Bower and Sawchuk shared the Vezina Trophy in 1964–65.

On April 6, 1969, at the age of 44 years, 4 months, and 29 days, Bower became the oldest goaltender to play in a Stanley Cup playoff game, a distinction previously held by Lester Patrick. He played his last game on December 10, 1969, a 6–3 loss to Montreal; mainly due to injuries, this was his only game of the 1969–70 season. At the time, he was the oldest full-time player to participate in an NHL game, and remains the second-oldest goaltender (45 years, 1 month, 2 days), behind only Maurice Roberts; he was surpassed as oldest full-time player by Gordie Howe, Chris Chelios, and Jaromír Jágr.

On March 19, 1970, Bower publicly announced his retirement, four months after his 45th birthday. He played eleven full seasons with the Leafs. When asked if he might reveal his true age, he replied “If you don’t know by now, you never will”. Coach Punch Imlach once told Bower, after seeing a purported birth certificate, “If you were born in this day here that you’re telling me, you had to be overseas with the First Division, in 1939, when you were 13.” Bower eventually revealed his birth date as November 8, 1924.

Bower was elected to the Hockey Hall of Fame in 1976, and to the AHL Hall of Fame as a member of its inaugural class in 2006. In 1998, he was ranked number 87 on The Hockey News’ list of the 100 Greatest NHL Players. He was inducted into the Etobicoke Sports Hall of Fame in 1994, and into the Ontario Sports Hall of Fame in 1999. He was married to Nancy and had a son, two daughters, eight grandchildren and six great-grandchildren, and resided in Mississauga, Ontario. After a city park near his house was renamed in his honour, he would routinely clean litter there, and feed the birds.

Bower worked for the Maple Leafs after his retirement in various capacities, including as a scout and a goalie coach. He was assistant coach for the Leafs from 1976 to 1978. He retired in 1990, but continued to make public appearances on behalf of the organization for the rest of his life.

In January 2004, Bower was featured on a postage stamp. As part of the NHL All-Stars Collection, he was immortalized along with five other All-Stars. In 2005, the Royal Canadian Mint featured Bower on a non-circulating fifty-cent coin, as part of its four-coin Legends of the Toronto Maple Leafs coin set. In 2007, it was announced that Bower would receive a star on Canada’s Walk of Fame.

On October 7, 2010, Bower opened the first game of the regular season for the Toronto Maple Leafs at Air Canada Centre by walking out on an implied “bridge over water” with his goalie stick.

On May 24, 2014, Bower attended a street renaming ceremony in Weston in Toronto. Patika Avenue, where he lived during the 1960s, was renamed Johnny Bower Boulevard. He said,”It’s a great day for me and my family…this is a better ovation than I used to get at Maple Leaf Gardens.”

On September 6, 2014, the Maple Leafs named him and Darryl Sittler two of the first three inductees of Legends Row (Ted Kennedy had been inducted some months earlier), with statues outside Air Canada Centre of twelve of the greatest players in Maple Leafs history.

On December 26, 2017, Bower died at the age of 93 from pneumonia. In the days following Bower’s death, many teams, including the Maple Leafs, Winnipeg Jets, Arizona Coyotes and Toronto Raptors of the National Basketball Association honoured Bower with pre-game tributes. On January 3, the Maple Leafs hosted a public celebration of Bower’s life at the Air Canada Centre. The event was attended by thousands, including various NHL alumni, members of the current Maple Leafs team and other major figures. The memorial was televised across several channels in Canada, and in accordance with the event, Toronto Mayor John Tory declared January 3 to be Johnny Bower Day in the city of Toronto. For the remainder of the 2017–18 season, the Maple Leafs wore patches on their jerseys and helmets in honour of Bower.