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Harold Perrineau as Boyd Stevens, the self-appointed sheriff and de facto mayor of the Township. He is a retired US Army veteran who served in Afghanistan and Iraq. Boyd is estranged from his son, Ellis, after killing his wife, Abby, who had a sudden mental breakdown and inexplicably killed a number of the townspeople.
Catalina Sandino Moreno as Tabitha Matthews, Jim's wife and Julie and Ethan's mother, who together are new arrivals to the town. She chooses to live in the Township with her husband and son and is still mourning the recent loss of her youngest child, Thomas. At the end of the third season, she is revealed to be a reincarnation of Miranda Kavanaugh.
Vivian Crooks portrays young Tabitha (guest seasons 3–4)
Sarah Booth as Miranda Kavanaugh (guest seasons 2–4), Tabitha's previous incarnation, who was Victor and Eloise's mother and Henry's wife, and was killed during Victor's childhood by the creatures
Eion Bailey as Jim Matthews (seasons 1–3; guest season 4), Tabitha's husband and Julie and Ethan's father, who lives in the Township with his wife and children. He works with Jade to find a way to escape the town and contact the outside world.
David Alpay as Jade Herrera, a wealthy software developer who arrives at the town on the same day as the Matthews family. Despite his intelligence, he is initially arrogant and abrasive to the Township residents and struggles with his new circumstances. At the end of the third season, he is revealed to be a reincarnation of Christopher. During the fourth season, Jade learns that all of his past incarnations were killed by the townspeople after discovering who he really was and blaming him.
Viggo Hanvelt portrays young Jade (guest season 4)
Thom Payne as Christopher (guest seasons 2–4), Jade's previous incarnation, who was a ventriloquist and resident of the Township during Victor's childhood
Dylan Bailey (guest seasons 1 and 4) and André Pettigrew (guest seasons 1 and 4) as previous incarnations of Jade and Christopher
Elizabeth Saunders as Donna Raines, the leader of the residents at Colony House, who live separately from the Township
Shaun Majumder as Father Rudra Khatri (season 1; guest seasons 2–4), the Township's Christian priest and voice of reason in the community. Following his death, he continues to appear before Boyd as a hallucination.
Scott McCord as Victor Kavanaugh, a peculiar Colony House resident trapped in the town since he was a child
Eli Arsenault portrays young Victor (guest seasons 1–3)
Ricky He as Kenny Liu, Boyd's deputy and right-hand man, who lives with his aging parents in the Township
Chloe Van Landschoot as Kristi Miller, the Township's doctor and a former medical student who was separated from her fiancée when she became trapped in the town
Pegah Ghafoori as Fatima Hassan, Ellis's girlfriend, later wife, and one of the Colony House residents. At the end of the fourth season, she gains the ability to transform into one of the creatures.
Corteon Moore as Ellis Stevens, Boyd's son, who lives estranged from his father at Colony House
Hannah Cheramy as Julie Matthews, Jim and Tabitha's teenage daughter and Ethan's older sister, who at first chooses to live at Colony House, where she befriends Ellis and Fatima
Simon Webster as Ethan Matthews, Jim and Tabitha's young son and Julie's younger brother, who lives with his parents in the Township
Avery Konrad as Sara Myers, Nathan's sister who works at the Township's diner. She has frequent hallucinations that command her to kill other residents of the Township.
Paul Zinno as Nathan Myers (season 1), Sara's brother, who lives in the Township and tends to the farmed animals
Elizabeth Moy as Tian-Chen Liu (seasons 1–3), Kenny's mother and Bing-Qian's wife, who runs the diner in the Township
Deborah Grover as Tillie (seasons 2–3), an aging, carefree woman and one of the bus passengers who arrive at the town
Angela Moore as Bakta (season 2–present), a bus driver who unknowingly brings many new arrivals to the town
Kaelen Ohm as Marielle Sinclair (seasons 2–4), Kristi's fiancée, a pediatric nurse, and one of the bus passengers who arrive at the town
A.J. Simmons as Randall Kirkland (season 2–present), a volatile, quick-to-anger man and one of the bus passengers who arrive at the town
Nathan D. Simmons as Elgin Williams (seasons 2–4), one of the bus passengers who had a prophetic dream about the town while arriving there. He is first contacted by the "Boy in White", and is later manipulated by the "Kimono Woman".
Robert Joy as Henry Kavanaugh (season 3–present), Victor's father, who lived alone in Camden, Maine, for forty years after the disappearance of his wife and children
Samantha Brown as Dani Acosta (season 3–present), a police officer brought to the town after picking up Tabitha and Henry in the outside world
Julia Doyle as Sophia (season 4), a new arrival at the town who presents as a sheltered and vulnerable pastor's daughter. Sophia is a disguise used by the shapeshifting "Man in Yellow" to infiltrate the townspeople.
Douglas E. Hughes as the "Man in Yellow" (recurring season 4; guest season 3), a powerful evil shapeshifting entity, who first contacted Jim over the radio at the end of the first season.
