Jasper is in the middle of Jasper National Park, in the province of Alberta. The town and the park, which draws more than two million tourists a year, were evacuated on Monday, when officials estimated there were 15,000 visitors in the park.
Environment Canada is forecasting 10 mm to 20 mm of rain for Thursday, which might help firefighters.
The blaze is one of hundreds ravaging the western provinces of Alberta and British Columbia. The federal government said in April that high temperatures and tinder dry forests meant this could be one of the worst years ever for fires in Canada.
Officials said the flames in Jasper reached a height of 400 feet and moved at 15 metres a minute.
"As the pictures and videos circulating online show, significant loss has occurred within the town site," Parks Canada said in a statement.
The federal government and other cities in Alberta are sending help. One major focus is the Trans Mountain oil pipeline, which can carry 890,000 barrels per day of oil from Edmonton to Vancouver.
"Losing structures, community, is like losing a close friend ... (but) the people have been saved and that is significant. We can find a way to rebuild," Jasper mayor Richard Ireland told the Canadian Broadcasting Corp.
One of the buildings destroyed by fire was the Maligne Lodge hotel in the south of the town.
"It's just so sad to know that so many families and people have lost not just their belongings but their livelihood and a beautiful park," owner Karyne Decore told the CBC.
There are currently 175 wildfires burning in Alberta, more than 50 of which are out of control.
The Jasper fire could be one of the most damaging in Alberta since a 2016 conflagration that hit the oil centre of Fort McMurray, forcing the evacuation of all 90,000 residents. The blaze destroyed 10 per cent of all structures in the city and shut in more than a million barrels per day of oil output.