The story takes place in Gilead, a “Puritan theocracy” established in place of the United States in the 21st Century, previously described in The Handmaid’s Tale. It interweaves narratives by Aunt Lydia, Agnes, and Nicole (who is initially known as Daisy).
Aunt Lydia, the most powerful Aunt in Gilead and one of its architects, writes that she is nearing the end of her life, and already many want her dead. However, she intends to take the entire country down with her when she dies. For years she has been compiling damning information about Gilead’s leadership and she is preparing to release it to the world. Her rival Aunt Vidala is constantly scheming against her, and Lydia needs to survive long enough to smuggle the information out of Gilead. Lydia spends her time planning and counteracting Vidala’s schemes, often by blackmailing or coercing other powerful people. She often meets with Commander Judd, one of Gilead’s most powerful officials, who is trying to uncover a secret traitor in their midst who is slowly leaking intel to an anti-Gilead resistance movement called Mayday. He does not suspect that the traitor is Lydia herself. Lydia also recalls her past life as a judge, and her days in Gilead’s founding when she was arrested, tortured, and then co-opted into designing much of Gilead’s social structure, especially as it pertains to women. Lydia complied, but even from Gilead’s formation began plotting her revenge.
As a young child in Gilead, Agnes enjoyed her days with her adoptive (though Agnes does not know it yet) mother Tabitha, Commander Kyle’s wife. As the only child of an elite family, Agnes is well cared for, but she is taught to fear men’s powerful sexual urges and thus her own sexual allure, even as a very young girl. These happy days end when Tabitha dies and Commander Kyle remarries a widow named Paula. Agnes soon discovers that Tabitha was not her real mother; her real mother is an escaped Handmaid, though no one knows what became of her. A few years later, Commander Kyle gets a Handmaid named Ofkyle to bear him a child since Paula, like most women, is infertile. Ofkyle becomes pregnant and gives birth, though when complications set in, the doctor cuts her open to retrieve the baby, killing her. Agnes is immensely disturbed that Ofkyle never gets to choose whether she lives or dies. When Agnes is entering puberty and marriageable age, she and her friend Becka are put into marital preparatory school and will soon be forced to marry much older men. They are both terrified by the prospect of marrying strangers and being forced to have sex with them, in part because they both have been victims of sexual abuse by Becka’s father, Dr. Grove. Becka is so mortified by the idea that she slashes her wrist, trying to commit suicide. Paramedics save her life, and Lydia offers Becka the option of becoming an Aunt instead, which means she will live in Ardua Hall and never marry. Becka accepts with gratitude, and Lydia notes that she may bank on that gratitude in the future. Meanwhile, Agnes is engaged to be married to Commander Judd. She considers trying to commit suicide like Becka, but lacks the resolve. Mere days before she is to be married, Lydia slyly suggests that Agnes can become an Aunt like Becka and herself and thus be spared from marriage, an offer which Agnes accepts. As Aunts, Becka and Agnes are allowed to live together and learn to read. Through reading the Bible and discovering criminal evidence against various people in Gilead’s leadership, they both realize that Gilead is overwhelmingly corrupt and rotten to the core.
In Toronto, Canada, Daisy lives with her parents Neil and Melanie, who run a secondhand clothes store called The Clothes Hound, though Daisy always feels strangely distant from them. On Daisy’s sixteenth birthday, a car bomb at the store kills both Neil and Melanie, and Melanie’s friend Ada takes Daisy on the run, where she learns that she is actually Baby Nicole, a famous child who was smuggled out of Gilead when she was an infant. Neil and Melanie were not her true parents, but rather operatives for the anti-Gilead resistance movement Mayday, which is why they were murdered by Gilead agents who are now hunting for Nicole herself. Nicole’s real parents are alive, but in hiding. Ada introduces Nicole to Mayday operatives Garth and Elijah, and they together explain that they have an unknown source in Gilead who promises that they have enough damning information to topple Gilead’s regime, but they need a way to get the information out to Canada. The source proposes that they send Nicole into Gilead, posing as a new convert, and then the source will give her the cache of information and smuggle her back out of the country. Nicole is scared of this plot, but is swept into it by the others, since this is their best chance of defeating Gilead. Garth teaches Nicole how to fight and survive and then takes her out to live on the streets with him for a week, until Gilead missionaries find them and take Nicole (who is now operating under the name Jade) back with them to Gilead. Jade is brought to Ardua Hall and placed under the care of Becka and Agnes, who are supposed to make a proper convert out of her. However, Jade is boisterous and unruly and does not blend in well to Gilead’s somber and modest culture.
When Jade is getting anxious, unsure how she is supposed to find the source, Lydia reveals herself to her and brings both Becka and Agnes into her plan. She reveals that Agnes and Nicole are half-sisters, daughters of the same escaped Handmaid. Lydia tells all of them that for the good of the women and children in Gilead, they must help it to fall. Lydia implants a piece of microdot film containing all of the criminal evidence she has gathered on Gilead’s government over several decades into Nicole’s arm. Her plan is for Agnes and Nicole to leave Gilead for Canada under the pretense of being new missionaries and with Nicole posing as Becka, while Becka herself remains in Gilead in Nicole’s place, hiding out in a retreat center. This will effectively require Becka to sacrifice herself for the mission and her friends, but Becka agrees to do so. However, Commander Judd and his men invade Ardua Hall, believing that the traitor is somewhere inside, which forces Agnes and Nicole to leave prematurely. There is no time for Becka to be protected from harm, so she hides on the roof and drowns herself in the cistern, rather than allowing herself to be captured and interrogated. While Agnes and Nicole are fleeing, they are discovered by Aunt Vidala, who realizes that a plot is afoot, but Nicole punches her in the chest so hard that her heart stops and she goes into a temporary coma. Agnes and Nicole travel on, passing through checkpoints as missionaries and being smuggled through New Hampshire and Maine into Canada by a series of individuals who hate Gilead and cooperate with Mayday. Though they nearly drown, Agnes and Nicole reach the shores of Canada and are picked up by Ada, Garth, and other Mayday operatives. The data is taken from Nicole’s arm and passed on to national news, which broadcasts it around the world. Agnes and Nicole finally meet their mother, who has been in hiding in Canada since they were both young children. Lydia ends her narrative knowing that her mission has succeeded, though she has now been discovered and intends to commit suicide with a morphine injection.
In the epilogue, a historian named Pieixoto speaks at a conference in 2197 and confirms that following the release of the damning information, Gilead fell to international pressure and local rebellions. He also suggests that Agnes and Nicole’s mother was Offred, the main character of The Handmaid’s Tale.
