Inspired by the novel of the same name by Margaret Atwood, The Handmaid's Tale is a dystopian series on an extremely patriarchal and totalitarian future in which 'handmaids' are forced to produce children for the ruling class. The show has made Elisabeth Moss (who plays the protagonist Offred/June) a household name while garnering similar acclaim for Yvonne Strahovski and marking a major acting comeback for Joseph Fiennes.

Apart from these actors, The Handmaid's Tale has also had its share of guest appearances featuring prominent character actors in small yet significant roles.

Updated on November 12th, 2022 by Colin McCormick: With The Handmaid's Tale returning for its fifth season, fans can rejoin the gripping dystopian story and its complex characters. But while the likes of Elizabeth Moss and Ann Dowd continue to lead the show as the main cast, there have been a number of other notable actors who have appeared in guest roles. From well established stars in brief appearances to newer talents who have become more renowned since appearing on the show, fans might not have known about these guest actors on The Handmaid's Tale.

Marisa Tomei

Marisa Tomei in The Handmaid's Tale

In her diverse career with dramas and comedies, Marisa Tomei has won an Academy Award for her supporting role in My Cousin Vinny. Modern-day audiences might know her mostly from her portrayal of Aunt May in the MCU.

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In the Season 2 episode titled Unwomen, Tomei plays Mrs. O'Conner, one of the Commanders' wives who lost her high rank in society for committing the sin of adultery. Even though she's shown to be a believer in her society's extremist values, she still has a few differences. She also believes God would ultimately forgive her for her affair was motivated by love. She's categorized as an 'unwoman', the lowest social class of women in the Gilead.

Mckenna Grace

mckenna grace handmaid's tale season 5 return

Mckenna Grace has impressed a lot of people with her very young career at this point. She has appeared in a recurring role on Young Sheldon while also taking roles in big Hollywood movies like Captain Marvel and I, Tonya. She found a breakout role in the popular legacy sequel Ghostbusters: Afterlife.

Mckenna first appears on The Handmaid's Tale in the show's fourth season as a young yet heroic wife inside Gilead. Esther takes in June and the other Handmaids, hiding them out in her farm. She returns in season 5, showing the consequences of her heroic deed.

Jim Cummings

Jim Cummings in The Handmaid's Tale

The Gilead's secret police force is known as the Eyes. One of its members is Burke who's briefly introduced in Season 1. Burke makes his rounds at Serena Joy's house, monitoring the activities and interactions of June. He leaves the place when he mistakenly thinks that June might be carrying a child for Serena, stating that he has all the information that he needed.

Director, writer, and actor Jim Cummings plays Burke. Cummings is mostly known for directing and starring in the 2018 comedy-drama Thunder Road that opened to rave reviews at American film festivals. His latest venture was a horror-comedy called The Wolf of Snow Hollow.

Laila Robbins

Jim Cummings in The Handmaid's Tale

On TV, Laila Robbins is popular as Katarina Rostova on The Blacklist, and Colonel Grace Mallory on The Boys. In the third season of The Handmaid's Tale, she has another dominant, and uptight role as Pamela Joy, mother of Serena Joy.

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Pamela is a Widow but despite the ostracized status of Widows in the Gilead, she manages her own household and enjoys considerable freedom. She constantly advises Serena to be a good wife to her Commander husband and to be a good mother so that she can enjoy the benefits of the unjust society they dwell in. She seems to lack all empathy as whenever Serena complains about her life, Pamela calls her a 'spoiled little girl'.

Clea DuVall

Sylvia and Emily putting their heads together in The Handmaid's Tale

Clea DuVall has been steadily working in movies and television for several decades now with early teen roles in The Faculty and Girl, Interrupted. She has appeared in small supporting roles in a number of acclaimed movies from Zodiac to Argo. And last year she directed the holiday comedy Happiest Season starring Kristen Stewart.

DuVall first appears in The Handmaid's Tale second season in a one-episode role. She plays Sylvia, the wife of Emily. Shown in a flashback, the couple and their child attempt to flee to Canada only for Emily to get stuck behind. Though Emily's story has ended on the show, Sylvia has returned to pick it up.

John Carroll Lynch

John Carroll Lynch in The Handmaid's Tale

Reputed character actor and American Horror Story regular John Carroll Lynch guest-starred as Dan in the show's sophomore season. Before the Gilead rose and took over the American government, Dan served as a college professor, also serving as Emily Malek's supervisor.

A gay man himself, Dan is seen as warning Emily of the future that she might face for her same-sex relationship as the Gilead wouldn't tolerate homosexuality of any kind. Both characters collectively decide to resist the homophobic policies of their academy until Dan is brutally murdered, with homophobic slurs painted around him.

Yahya Abdul-Mateen II

Yahya Abdul Mateen II in The Handmaid's Tale

Yahya Abdul-Mateen II appeared in Season 2 as Omar. He's a member of the resistance movement that helped people escape from the Gilead. He also helps June escape to a safe house, also offering her refuge in his own house.

The actor was relatively unknown by the second season but he gained more attention with meatier roles. He won an Emmy for playing Dr. Manhattan in HBO's Watchmen miniseries while also appearing in The Matrix Resurrections and Candyman. Though his DCEU spinoff is stuck in development hell, he will return as Black Manta in Aquaman and the Lost Kingdom.

Oprah Winfrey

Oprah Winfrey

Even Oprah Winfrey makes her way into The Handmaid's Tale, making an uncredited voice appearance as a newsreader in Season 2. More specifically, the reputed talk show host and philanthropist plays a radio show host in the 11th episode titled Holly.

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Showrunner Bruce Miller explained her casting as: 'The radio segment she recorded was inspired by the free radio of the Allies from World War II. It was an absolute honor to have Oprah featured on the show, and especially thrilling as she was the one who presented us with the Emmy last year."

Zawe Ashton

Zawe Ashton smiling as Oona in The Handmaid's Tale

Zawe Ashton is an up-and-coming talent who is sure to get a lot of attention very soon. To date, she is perhaps best known for roles in the thrillers Velvet Buzzsaw and Nocturnal Animals. However, Ashton's biggest role yet is still ahead as she will play the villain in the upcoming The Marvels, one of the MCU's most exciting Phase 5 movies.

Ashton appears as Oona in season 4 of The Handmaid's Tale. Oona is a British woman living in Toronto and helping out with the aid and refugees from Gilead. She is also in a relationship with Moira which is tested due to the risks of helping June escape.

Zabryna Guevara

Zabryna Guevara in The Handmaid's Tale

In Season 1, Zabryna Guevara appears as Ambassador Castillo, a Mexican ambassador who visits Selena's home and is briefed by the Commanders about the efficiency of the Gilead regime. Castillo also questions June, asking her if being a Handmaid was her conscious choice. To this, she blatantly lies that she has found happiness in this position.

Guevara might be known to fans of Gotham as Sarah Essen, the captain of Gotham City Police Department's Homicide Squad. She also appeared as Maret in the Stephen King anthology series Castle Rock.

Rebecca Rittenhouse

Oddette in The Handmaid's Tale

Rebecca Rittenhouse plays Odette, a doctor who appears in the flashback sequences in Season 2. She helped Moira with her pregnancy and later also engaged in a relationship with her. Because of her sexual identity, Odette was rounded up as an 'unwoman' by the Gilead and executed by the state.

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Gaining fame as Dr. Anna Ziev in The Mindy Project, Rebecca Rittenhouse was last seen as actress Michelle Phillips in Quentin Tarantino's ninth film, Once Upon A Time In Hollywood.

Christopher Meloni

Commander George Winslow in The Handmaid's Tale

Many fans will know Christopher Meloni best for his role as Detective Elliot Stabler on Law & Order: SVU. Though he left the show abruptly in the show's 12th season, making for one of the worst television exits according to fans. However, he returned to the role of Stabler in Law & Order: Organized Crime.

In season 4 of The Handmaid's Tale, Meloni plays George Winslow. As one of the commanders inside Gilead, he is willing to take drastic measures to ensure it thrives. But his confrontation with June leads to a shocking conclusion.

Sydney Sweeney

Eden talking outside to Nick on The Handmaid's Tale.

With Euphoria's Cassie Howard becoming a breakout television character in 2022, actor Sydney Sweeney looks poised to become a big star in Hollywood. The actor recently scored Emmy nominations for her performances in Euphoria and The White Lotus. She also has some huge upcoming projects like Madame Web and Barbarella.

Sweeney plays Eden in season 2 of The Handmaid's Tale, completing a complex and tragic arc as the character. She is initially a true believer who happily accepts her role as Nick's wife only to discover love outside of the marriage and questioning everything.

Amy Landecker

Amy Landecker in The Handmaid's Tale

The actress is popular for playing Sarah in the Amazon Prime series Transparent, as well as supporting roles in films like Dan In Real Life, and A Serious Man. Her recent film appearance was in Project Power. Amy Landecker plays a minor character called Mrs. MacKenzie in the second and third seasons of The Handmaid's Tale.

She is the wife of Commander MacKenzie as serves as the placement mother to Hannah, June's daughter. She's a kind-hearted, middle-aged woman who is never harsh towards her adoptive daughter whom she renames Agnes.

John Ortiz

John Ortiz in The Handmaid's Tale

John Ortiz has a plethora of character roles in his versatile filmography as a film and TV actor. He has also appeared in franchises like Fast & Furious. In Season 3, he's introduced as Jim Thorne, a widowed principal of the same school in which Lydia Clements (aka Aunt Lydia) taught before the Gilead took over the state.

Lydia spent a night partying with Jim, proceeding to get intimate further before Jim said that it's too soon for him to engage in such a relationship after his wife's death. Lydia cries out of embarrassment and ends up taking out her frustration on one of the single mothers of her students, handing her to the authorities terming her unfit to take care of a child.

NEXT: The Handmaid's Tale Characters, Ranked By Kill Count