Jean Smart won her fifth best actress award for the fifth and final season of Hacks and Noah Wyle made it two for two as best actor in a drama for The Pitt.
Australia's Sarah Snook was nominated for thriller All Her Fault but lost to Hollywood veteran Sally Field.
Field, 79, became the oldest woman to win best actress in a limited or anthology series or TV movie for Remarkably Bright Creatures.
The Apple TV horror comedy Widow's Bay rode into the night on a wave of buzz. It had already won eight Emmys at an earlier ceremony and added four more, including supporting actress for breakout star Kate O'Flynn and supporting actor for Stephen Root.
Rhys also won best actor in a limited series for The Beast in Me, becoming the first man to win two leading actor categories in the same year.
"The celebrations will be long, varied, and I hope at times wild," Rhys said backstage while holding both Emmys.
It also won for directing for Hiro Murai and for writing for its creator Dippold, a first-time Emmy winner and first-time nominee who was previously best known for an old viral tweet showing her dressed as The Babadook.
If it wins best comedy series, Widow's Bay would break the record for Emmys in a comedy that The Studio set in 2025 with 13.
Smart's fifth win was an unprecedented sweep. No actor had won an Emmy every year for a series that lasted more than three seasons until she did it on Monday.
"What a ride this has been," an emotional Smart said after getting a standing ovation.
The 75-year-old Smart has won eight Emmys overall in a career that was already more than respectable when she landed her defining role of Deborah Vance, a brash stand-up comic pushing back against age, obscurity and sexism in the HBO Max series.
Wyle won the Emmy for the second season of The Pitt, HBO Max's real-time emergency room drama, for playing Dr Michael "Robby" Robinavitch, a role that brought him a major career revival after starring in ER in the 1990s.
"I grew up in LA, I'm a Hollywood kid. I was raised on a television, and movie theatres were my place of worship," Wyle said in his acceptance.
"This is all I've ever wanted to do, and this is the only club I've ever wanted to join."
O'Flynn, a 40-year-old British actor whose previous acclaim came mostly for her work in theatre, plays Patricia Moyer, a city worker and social outcast dealing with a demonic darkness on Widow's Bay.
"This is the role of a lifetime," O'Flynn said.
"This is for all the Patricias out there."
Root, one of the most ubiquitous character actors of the last few decades, beat out Harrison Ford, who many thought would get his first major competitive Hollywood award for his role on Shrinking.
"Thank you, sir, for all your many years of great, great, great acting," Root said to Ford during his acceptance.
The Pitt was the top overall nominee, but it lost in both supporting acting categories despite having four nominees in one of them and three in the other.
Allison Janney won best supporting actress in a drama over Katherine LaNasa from The Pitt, who won last year, and three of her castmates. Janney joined Smart as an eight-time Emmy winner.
Tom Pelphrey won supporting actor in a drama for Task.
The Late Show with Stephen Colbert, taken off the air by CBS, won best variety series.
It's one of six Emmys the show has won this year after the show was cancelled for what the network said was economic reasons while many believe it was his criticism of the Trump administration.
"If you like the comedy tonight, my old writers wrote it," Colbert said.
Mariska Hargitay opened the NBC telecast with a musical tribute to television.
"NBC is celebrating its 100th year, and I have been on 'Law & Order: SVU' for all of them," said Hargitay, a three-time Emmy winner who has starred in the show for 27 seasons.
Taylor Swift acted alongside Hargitay in a pre-recorded Law & Order-based bit during the show.
Michael J Fox, the actor who turned his Parkinson's disease diagnosis into one of entertainment's most influential advocacy campaigns, received the Bob Hope Humanitarian Award.
Fox, 65, returned from retirement to appear in Shrinking, earning his 19th Emmy nomination while continuing the Parkinson's disease advocacy and research efforts that prompted the Television Academy to honour him.
The academy recognised him for "his transformative contributions to Parkinson's disease research and advocacy".
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