Sarah Snook, Kieran Culkin, and Matthew Macfadyen all won acting prizes for
Succession, while the show also won best drama series overall.
Creator Jesse Armstrong said it was "a great sadness to end the show, but it was a great pleasure to do it".
Also at the ceremony, Sir Elton John won his first Emmy Award, finally giving him EGOT status.
That means he has joined an exclusive club of performers who have won an Emmy, Grammy, Oscar and Tony award.
Elton Live: Farewell From Dodger Stadium won best variety special live, marking the British singer-songwriter's first Emmy nomination and award.
However, Sir Elton could not pick up the honour after having a knee operation.
A spokesperson accepted the trophy on his behalf, describing the win as "historic" and saying Sir Elton had "created the soundtrack to all of our lives [and] has done so much great for society".
Other winners of the night included The White Lotus and Abbott Elementary.
Succession, the critically acclaimed drama about a media mogul and the power struggles between his dysfunctional family, concluded last year after four seasons.
It was rewarded generously at the Emmys, winning best drama series and prizes for writing and directing, while Snook and Culkin won best leading actress and actor respectively.
"The bar was set so high and that was what spurred us on," Snook said of Succession's success.
She also thanked her parents, telling them: "Mum and dad - thank you for having a dress-up box when I was a kid, this is where it gets you!"
Snook dedicated the award to her daughter, with whom she was pregnant while filming. "It's very easy to act when you're pregnant because you've got hormones raging," she joked.
Her co-star Kieran Culkin paid tribute to Armstrong "for being a brilliant writer, showrunner and gentleman".
Culkin also thanked his mother and manager as well as his wife Jazz and their two children, before addressing his wife from the stage: "And Jazz, I want more [children]. You said maybe, if I won!"
In his own acceptance speech: Macfadyen joked: "I must make special mention to my on-screen wife Sarah Snook, and my other on-screen wife Nicholas Braun."
Braun, a fellow nominee, plays Cousin Greg in Succession, and the two characters' relationship was a favourite with viewers.
"Acting with you has been one of the most wonderful things in my career, so thank you Nick, thank you Sarah," Macfadyen added.
Armstrong, the British screenwriter who created the series, also scooped the top prize for best writing in a drama series.
In his speech, Armstrong referred back to the main plotline, joking: "For some reason, the name of a certain Australia-born media mogul, Rupert Murdoch, springs to mind."
He added: "I come from the UK and the show is about things that are close to the centre of American life and politics, and we've always been met with generosity and good faith and that's part of America's tradition of being very welcoming to outsiders."
Elsewhere, The Bear won three acting prizes, for its star Jeremy Allen White, and supporting actors Ayo Edebiri and Ebon Moss-Bachrach.
Accepting his award, White said: "I am so full of gratitude to be standing in front of you all - I love this show so much, it filled me up, set a fire in me."
Edebiri told the audience she was "so incredibly grateful for so many reasons".
"This is a show about found family and real family, and my parents are here tonight - thank you so much for loving me and letting me feel beautiful and black and proud of all of that," she said.
While Succession and The Bear won six prizes each in the drama and comedy categories respectively, Netflix's road rage-inspired series Beef dominated the limited series categories.
Ali Wong and Steven Yeun, the show's two stars, were named best actress and actor in a limited series respectively.
Accepting the prize for best limited series, creator Lee Sung Jin said: "I'm really grateful and humbled by everyone who watched the show and reached out about their own personal struggles, it's very life-affirming, so thank you."
He concluded his speech by joking: "Everything I do is for my three dogs."
Several winners picked up their prizes just a week after winning similar trophies at the Golden Globes - including Snook, Culkin, Edebiri, White, Yeun and Wong.
Quinta Brunson won the prize for best leading comedy actress for her role in school-based series Abbott Elementary.
In an emotional speech, Brunson said she was "so happy to be able to live my dream and act out comedy".
Jennifer Coolidge was named best supporting drama actress for her role in privilege satire The White Lotus.
In her acceptance speech, Coolidge joked that she wanted to "thank all the evil gays" - a reference to her storyline in the second season of The White Lotus.
Niecy Nash-Betts won best supporting actress in a limited series for Monster: The Jeffrey Dahmer Story.
She said: "I accept this award on behalf of every black and brown woman who has gone unheard yet over policed - like Glenda Cleveland, like Sandra Bland, like Breonna Taylor.
Cleveland, who Nash-Betts plays in the series, was the woman who alerted the police about the serial killer.
The ceremony also saw Charlie Puth perform the theme tune to Friends as the Emmy Awards remembered those who have died in the industry, including Matthew Perry.
The Emmys, which were presented by actor and comedian Anthony Anderson, were delayed by four months due to the Hollywood strikes.
Nominations were announced in July and the ceremony was originally scheduled for September, but the writers' and actors' strikes meant very few nominees would have been able to attend.
Source: BBC News
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