The team were whistled off the pitch and fan expectations heading into next Thursday's opening match are low.
Putin said in an interview posted on the Kremlin website today that he expected the national squad to play with courage and flair.
"As far as the team are concerned, I must acknowledge the fact that, unfortunately, our team have not achieved big results in recent times," Putin said.
"But we very much expect -- all fans and lovers of football in Russia -- expect the team to play with dignity, for them to show modern, interesting football, and to fight until the end."
The hosts are expected to vie with outsiders Saudi Arabia and Egypt for the runner-up spot in a group that includes two-time World Cup winner Uruguay and earn a place in the last 16.
Russia have never made the knockout stage of a World Cup as an independent nations and are desperate to make amends at home.
But Cherchesov's men have been decimated by injuries and forced to change lineups and formations from game to game.
Putin said Russia's biggest achievement may simply be pulling off a successful World Cup.
"Our main goal as tournament organiser is to conduct the World Cup with dignity, to make it into a celebration for millions of football lovers all over the world," he said.
"This will be our biggest achievement."
Putin also tried to play it coy when pressed on whom he thought would win the showpiece when the final is played in Moscow on July 15.
"This is a difficult question. There are many contenders," said Putin.
"There are the Latin American countries -- Argentina and Brazil. We know that Germany played brilliantly in previous World Cups.
"The Spanish team showed some high-quality, beautiful football. I am sure there will be other contenders. But the strongest will win."
Putin was not asked what would happen if the hosts failed to make it out of one of the easier groups in the draw.
But Russian Sport Minister Pavel Kolobkov said in late May that qualification for the knockout stage was a must.
"The first thing we have to do is make it out of the group," Kolobkov told Russian state television.
"That is not even up for discussion.