"Last night Gord quietly passed away with his beloved children and family close by", his heartbroken family wrote in a statement.
Canadian Prime Minister Justin Trudeau tweeted this Wednesday morning: "There will never be another like you, Gord".
"He loved every hidden corner, every aspect of this country that he celebrated his whole life".
"He wanted to make it better". "He knew, as great as we were, we needed to be better than we are", he added.
After three decades of making music with his former high school mates, Downie's doctors made public his condition in May 2016, saying he had rebounded after undergoing surgery and chemotherapy but that the cancer was "incurable", prompting an outpouring of support.
In a 2016 interview with the Canadian Broadcast Corporation, Dr. James Perry talked about accompanying Downie on his final tour from the dual perspectives of an oncologist and lifelong fan of The Tragically Hip.
The city demonstrated its love for Downie a year ago when it set up giant screens in Gage Park to broadcast the Hip's final concert on CBC.
Its discography sold more than eight million copies, appealing to partiers and intellectuals alike.
"Gord knew this [reconciliation] wouldn't be easy, but I pray that my friend has inspired us all to get moving", said Alvin Fiddler, Grand Chief of the Nishbawbe Aski Nation, in a statement.
In 2005, The Hip was inducted into the Canadian Music Hall of Fame at the Juno Awards Show in Winnipeg, cementing the band's place in this country's music history.
Tributes to the late singer poured in on social media.
As news of Downie's death began filtering in Wednesday, many Indigenous organizations and ordinary Canadians alike took to Twitter to remember his contributions.
"Today, he begins a new journey among the stars, but his music, his art, his work and his memory will always be with us", Bellegarde said. Last month, meanwhile, Long Time Running, a documentary about the band, was debuted and Downie announced his latest solo LP, "Introduce Yerself", would be arriving on October 27.