Dusmatov's win by unanimous decision over Bennama was especially crushing for French fans, coming a day after fellow Frenchman Sofiane Oumiha's loss in the lightweight final.
Junior Alcantara of the Dominican Republic and Cape Verde's David de Pina took bronze after their semi-final defeats.
French fans flooded into Court Philippe Chatrier to support Bennama and loudly shouted "allez les bleus" ahead of the bout, while booing Dusmatov on his entry.
The pair also faced off in the men's flyweight final at last year's world championships in Tashkent, which Bennama lost after being dropped to the canvas in the first round when he was struck with a firm right hand.
European Games champion Bennama adopted a more cautious approach this time around, which appeared to be working in his favour early on until Dusmatov landed two big left hands to take the first round 3-2.
Dusmatov did not let up in the second round and despite facing a taller opponent, connected with a few overhand left hands to also take the second.
With his gold medal hopes evaporating in front of his eyes, Bennama went all out in the final round and breathed some life back into a deflated crowd, but Dusmatov showed his experience by keeping out of range and letting fly with stinging counters to win his second Olympic gold.
"I want to thank everybody back home who has supported me," said Dusmatov, who boxed as a professional from 2019-2023 and won all six of his bouts.
"After Rio, I took a little break in my Olympic career... This gold is more valuable (than Rio) because nobody thought I could achieve this. I have shown them that it was possible and at what level I can box."
Bennama said he did not view his silver medal as a disappointment.
"An indescribable atmosphere that helped me to go beyond my limits and I'm proud that I fought for them and to bring a beautiful silver medal for them. I'm satisfied with the work I've done," Bennama told France TV.
"I want to come back to go get this beautiful gold medal because I know what it means, so I think I'll be part of the party in Los Angeles."
Bennama had been looking to become the seventh French boxer to win an Olympic gold medal after Paul Fritsch in 1920, Jean Despeaux and Roger Michelot in 1936, Brahim Asloum (2000), Estelle Mossely and Tony Yoka (2016).
NIGHT OF FIRSTS
Earlier, Ngamba lost her women's middleweight semi-final to Atheyna Bylon of Panama by a 4-1 split decision.
Despite the defeat, Ngamba made history by becoming the first representative of the Refugee Olympic Team to win a medal at the Games, taking home bronze for reaching the semi-finals.
Ngamba was born in Cameroon and has lived in England for 15 years but is still awaiting citizenship.
She was arrested and faced the threat of deportation to West Africa, and has had to provide proof of her sexuality to immigration officials after coming out as gay and before securing refugee status.
The Refugee Olympic Team, made up of 37 athletes, was set up in 2016 to represent millions of displaced people across the globe.
Ngamba's opponent Bylon, who is guaranteed to become the first woman from Panama to win an Olympic medal, faces Li Qian in the final after the Chinese boxer claimed a unanimous win over Australia's Caitlin Parker.
Parker's defeat marked a difficult day for Australia and added to her compatriot Charlie Senior's defeat in the men's featherweight semi-finals against Uzbek Abdumalik Khalokov.
Australia, who arrived at the Games with the largest contingent of boxers (12), ended their campaign at the Olympic boxing tournament with two bronze medals.
In the other final on Thursday, bantamweight Chang Yuan became the first woman boxer to win Olympic gold for China by beating Turkey's Hatice Akbas.
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