The Testaments is the long-awaited sequel to TheHandmaid's Tale. The novel takes place approximately fifteen years after the events of The Handmaid's Tale and alternates between the perspectives of Aunt Lydia, one of the founders of Gilead; Agnes Jemima, a young woman who was raised under the Gilead regime; and Daisy, a teenager who was smuggled out of Gilead and now lives in Toronto.

Aunt Lydia's perspective is conveyed through illegal journal entries. It is clear from early in her narrative that she no longer possesses the illusion that Gilead represents a better, Christian society. Readers learn that Aunt Lydia was a court lawyer before the fall of the United States government. Gilead was able to gain power due to societal instability resulting from a steep decline in fertility and a worldwide environmental crisis. After a violent government takeover, Aunt Lydia became one of three founders of Gilead, tasked with writing the laws pertaining to women, essentially stripping them of human and reproductive rights.

Aunt Lydia is regarded as saint-like in Gilead society, and her followers offer contraband gifts to a statue in her likeness. She is instrumental in the creation of the Pearl Girls, young women who aspire to become Aunts and recruit new members to Gilead in Canada. Aunt Lydia reveals, however, that she is also a major May Day operative, a member of the resistance operating inside of Gilead. For years, Aunt Lydia has been accumulating evidence of corruption among the leaders of Gilead and passing on information to members of the resistance. While appearing to be the devout servant of Commander Judd, the leader of Gilead, she successfully orchestrates a mission to place Daisy in Ardua Hall as a Pearl Girl to act as a spy. Lydia tells Commander Judd that Baby Nicole has entered Gilead. Daisy smuggles information on high crimes committed by Gilead's elite, leading to the implosion of the regime. It is unclear whether Aunt Lydia survives its downfall. In the epilogue one hundred years later, Aunt Lydia is not mentioned, and little evidence of Gilead remains.

Agnes Jemima recounts having been raised by Commander Kyle and Tabitha, who was not her biological mother—Agnes Jemima, like all of Gilead's children, was birthed by a handmaid. As a child, she was devastated by her mother's death, and she frequently recalls Ofkyle, the family's handmaid who died during childbirth. She strongly dislikes her father's second wife, Paula, who became a widow under suspicious circumstances involving the murder of her husband. Agnes Jemima receives her education at Rubies Premarital Prepatory and begins preparing for her wedding at the age of thirteen. Refusing to marry, however, she seeks help from Aunt Lydia and became an Aunt in training at Ardua Hall.

Upon arriving at Ardua Hall, Agnes Jemima is reunited with her childhood friend Becka, whom she has not seen since her suicide attempt at preparatory school in order to avoid marriage. Before entering Ardua Hall, Agnes Jemima was sexually harassed by the town dentist, Dr. Grove—Becka's father. She learns that Becka had been raped by her father since childhood and developed a fear of marriage and sexual intercourse. After several years training as an Aunt, Agnes Jemima gains access to the library and reads the Bible for the first time. She comes to the understanding that her religious education during childhood was a lie perpetuated by Gilead and that their teachings about the Bible and God were false. Aunt Lydia secretly passes files on the crimes of Gilead's leaders to Agnes Jemima, which helps convince Agnes Jemima to join the resistance. Agnes Jemima and...