Mayor Greg Brackenridge said Whittaker will receive a hero's welcome on his return to the West Midlands - and had "earned a day with the mayoral chains".
Mr Brackenridge said he had been inundated with phone calls since Whittaker, from Darlaston, joked after his quarter-final fight that he wanted to "become the mayor of Wolverhampton" if he won gold.
The boxer's cheeky post-fight interviews have been among the memorable moments of the Tokyo games and Whittaker, whose father Tony Wilson works for Wolverhampton Council, has gained thousands of fans with his run to the Olympic final.
The disappointment was etched across the 24-year-old's face as he stood on the podium to receive his silver medal. He said he felt like a failure in an emotional interview afterwards and apologised for "letting down" the people of the West Midlands.
Wolves fan Whittaker lost a split decision to Cuba's Arlen Lopez in the men's light-heavyweight category on Wednesday morning.
His father Tony, who works at the city council and Wolves on matchdays, said he couldn’t be prouder of his son for what he had achieved.
He said it was difficult watching his son on the verge of tears after the heartbreaking defeat on the other side of the world but that there would be a big party for the young boxer when he returns home.
A strong start from the Cuban left Whittaker with a mountain to climb and while he edged the final round of the three-round contest, Lopez won gold after getting the nod from four of the five judges.
After watching the fight at his home, Mr Brackenridge admitted it was "bittersweet" to see 24-year-old Whittaker win silver.
He added: "There is disappointment of course because you always want to win, but I think he has done us all very, very proud.
"He's really put us on the map - he's managed to win a silver and we are really proud of him.
"My phone has not stopped ringing since Ben made his comment a few days ago."
Mr Brackenridge, who has offered to let Whittaker attend an official function and don the mayoral chains on his return to Wolverhampton, said: "He's going to get a hero's welcome. Of course we are going to be doing that.
"I think he has earned a day with the mayoral chains."
Heavyweight champion Anthony Joshua was among stars to show his support for Whittaker, liking his Instagram status in which he said: "Disappointment, embarrassment, the list goes on...".
He thanked people from the West Midlands and the country as a whole for their support during the Games.
Wolverhampton's Firewalker boxing club said in a statement that everyone there was proud of what Whittaker had achieved in Tokyo.
The statement, posted on the club's Facebook page, said: "He has shown the world that a young boy from Darlaston can not only compete on the world stage but also come home with an Olympic silver medal.
"Huge respect to everyone who has been a part of his journey."