The novel alternates among the perspectives of three women, presented as portions of a manuscript written by one (the
Ardua Hall Holograph) and testimonies by the other two. Lydia, a divorced judge, is imprisoned with other women in a stadium during the establishment of the Republic of Gilead, a
theonomic state. After enduring weeks of squalid conditions, torture, and solitary confinement, culminating in coerced participation in an execution, she and a small group of other women are handpicked by Commander Judd and Vidala, a pre-existing supporter of Gilead, to become Aunts—an elite group of women tasked with creating and overseeing the laws and uniforms governing Gilead's women. The Aunts use Ardua Hall as their headquarters and enjoy certain privileges that include reading "forbidden" texts, such as
Cardinal John Henry Newman's
Apologia Pro Vita Sua. In secret, Aunt Lydia despises Gilead and becomes a
mole supplying critical information to the Mayday resistance organization. Fifteen years after the events of ''The Handmaid's Tale'', a girl named Agnes Jemima is growing up in
Boston as the adopted daughter of Commander Kyle and his wife Tabitha. Agnes has a loving relationship with Tabitha, who later dies of ill health. Agnes and her classmates, Becka and Shunammite, attend an elite preparatory school for the daughters of Commanders, where they are taught to run a household, but not to become
literate. Once widowed, Commander Kyle marries Paula, the widow of a deceased Commander, who despises Agnes. Desiring a child for herself, she acquires a Handmaid, who successfully conceives but later dies giving birth to a son. Agnes is arranged to be married to Commander Judd, now a high-ranking official in charge of the Eyes and surveilling the population of Gilead. Learning that she is the daughter of a Handmaid, Agnes manages to escape her arranged marriage by becoming a Supplicant, a prospective Aunt. In that pursuit, she joins Becka, whose father — Doctor Grove, a prominent dentist — has been sexually abusing her and his other underage female patients for years. Later, Agnes is anonymously provided with files highlighting the corruption and hypocrisy at the heart of Gilead, specifically evidence of adultery between Commander Kyle and Paula and their plots to murder their respective spouses, and of Commander Judd's murders of his previous wives since divorce is prohibited. She also learns that she is the half-sister of "Baby Nicole", a girl who was smuggled out of Gilead to Canada by her Handmaid mother when she was young (and whose return the government of Gilead has been demanding). Meanwhile, a girl named Daisy — several years younger than Agnes — grows up in
Toronto with her parents, Neil and Melanie. The couple owns a second-hand clothes shop serving as a front for Mayday to smuggle women out of Gilead. On her 16th birthday, Neil and Melanie are murdered by undercover Gileadean operatives. Daisy is spirited into hiding by several Mayday operatives, who reveal that Neil and Melanie were not her biological parents and that she is actually Nicole. The Mayday operatives enlist her in a mission to infiltrate Gilead to obtain valuable intelligence from their mysterious mole. Nicole poses as a street urchin named Jade to be recruited by the Pearl Girls (Gilead missionaries who lure foreign women to Gilead with the promise of a better life), who take her up and bring her into Gilead. The disguised Nicole is placed under the care of Agnes and Becka, who are now respectively named Aunts Victoria and Immortelle. Aunt Lydia confirms that "Jade" is Nicole through a tattoo and discloses her true identity and parentage to Agnes and Becka. Revealing herself as Mayday's mole, Aunt Lydia enlists the three young women to smuggle incriminating information about Gilead's elite into
Canada. Nicole is tasked with carrying the files inside a
microdot on her cruciform tattoo. Agnes and Nicole are to enter Canada disguised as Pearl Girls, with Nicole and Becka swapping identities and Becka attending a
retreat to provide cover. Forced to hasten their plans when Commander Judd learns about Nicole's presence and intends to marry her, Agnes and Nicole set out early, assaulting Aunt Vidala and sending her to a hospital. They travel by bus and on foot, then by boat along the
Penobscot River. This boat takes them to a larger vessel, which brings them into Canadian waters, from which they reach
Campobello Island via inflatable and are picked up by a Mayday team and reunited with their mother. Meanwhile, Aunt Lydia, to buy Agnes and Nicole some more time and to secure her own position at Ardua Hall, tells Aunt Elizabeth that Aunt Vidala has accused her of the assault, expecting Elizabeth to kill Vidala. Using the contents of Nicole's microdot, the Canadian media leaks scandalous information about Gilead's elite, which leads to a purge that in turn causes a military
coup and popular revolt, weakening Gilead and leading to its fall and the restoration of the USA at the hands of Mayday and the US holdouts. Becka is found dead inside a water cistern, having hidden there to perpetuate the ruse that "Jade" had run off with a plumber. Lydia, the author of the
Ardua Hall Holograph, closes her story by describing her plan to commit suicide with a
morphine overdose before she can be questioned and executed. The novel concludes with a
metafictional
epilogue, described as a partial transcript at the Thirteenth Symposium on Gileadean Studies in 2197, presented by Professor James Darcy Pieixoto. He discusses the challenges in verifying the authenticity of the
Ardua Hall Holograph and the two witness transcripts by Agnes and Nicole. He also speculates that Agnes and Nicole's Handmaid mother could be Offred of the previous book, though he himself admits to not being sure, and that Aunt Lydia being the Mayday operative was just a cover to protect the real operative's identity. He concludes by mentioning a statue that was made commemorating Becka for her actions, its dedication having been attended by Agnes and Nicole, their husbands and children, their mother and their respective fathers. ==Characters==