The show also doffed its hat to diversity, giving Riz Ahmed the Outstanding Lead Actor in a Limited Series Award for "The Night Of" and the Best Actor in a Drama Series Award to "This Is Us" star Sterling K Brown.
"The Handmaid's Tale" bagged a total of eight awards out of its 13 nominations, including four in major categories such as the Best Drama Series, Best Director for Reed Morano, Best Actress for Elisabeth Moss and Best Supporting Actress for Ann Dowd.
Morano, who helmed the first three episodes of the show, became the first woman to win the Best Directing in a Drama Series in 22 years.
The Hulu show is set in the dystopian world of Gilead, a totalitarian society ruled by a fundamentalism regime that treats women as property of the state.
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"Margaret Atwood thank you for what you did in 1985 and thank you for what you continue to do for all of us," she said.
HBO's "Big Little Lies" dominated the Limited Series categories with eight awards, taking home the Best Actress, (Nicole Kidman), Supporting Actress (Laura Dern), Supporting Actor (Alexander Skarsgard), Director (Jean-Marc Vallee) and the Best Limited Series.
Accepting the award for Outstanding Limited Series, Kidman said, "The power of television has astounded us, you allowed us into your living rooms... But as much as the show has the entertainment value, it's about the issues."
"It has been an incredible year for women. Can I just say bring women to the front of their own stories, and make them the hero of their own stories," she added.
Writer-actor Lena Waithe made history by becoming the first black woman to win for comedy writing.
Waithe won the award for co-writing the "Thanksgiving" episode of "Master of None" with series co-creator and star, Aziz Ansari.
Waithe thanked her LGBTQIA family in her acceptance speech.
"It means a lot to me to be a first. It says that it's possible. I hope it gives other funny women of colour an opportunity because this door has now been opened. Give women of colour a seat at the table - and if you do that, you get one of these!," she said backstage.
Created by Armando Iannucci, "Veep", also won one of the night's top prizes for Best Comedy Series.
"Saturday Night Live" won the maximum of nine awards taking home the trophy for variety sketch series (its third overall in the category), Supporting Actor for Alec Baldwin for his role as President Donald Trump and Supporting Actress for Kate McKinnon, who portrayed Hillary Clinton, among others, in season 43.
Apart from women, artistes of colour also won in various major categories.
The last black actor who won the Lead Actor in a Drama series trophy was Andre Braugher for "Homicide" back in 1998.
Brown plays Randall Pearson, the black adopted son of the otherwise white Pearson family in "This Is Us", who is on a mission to find his biological father and explore his racial identity.
"I just want to say Mr Braugher, whether at Stanford University or on this Emmy stage, it is my supreme honour to follow in your steps," he said.
"I want to say it is always strange reaping the rewards of a story that's based on real world suffering, but if this show has shown a light on some of the prejudice in our societies, Islamophobia, some of the injustice in our justice system, then maybe that is something," he said.
Ahmed's Nasir Khan, on "The Night Of," is a Pakistani college student who winds up in jail after becoming involved in a murder investigation.
Atlanta's Donald Glover, who accepted the Emmy for the Lead Actor in a Comedy Series as well as the Best Directing for a Comedy Series, also became the first African-American to win in the directing category.
Colbert's hosting gig at the awards show was loaded with jokes about the president, whom he referred to as the "biggest TV personality of the year", adding "every show was influenced by Donald Trump in some way... All the late night shows obviously... "House of Cards", the new "American Horror Story".
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