The novel opens with a prologue during a conference championship football game. Ben Ressler, a celebrated National Football League (NFL) free safety, plays a fourth-quarter defensive series in freezing conditions. In total concentration, Ben reads the quarterback's eyes, tracks a pass, and launches himself into the tight end just as the receiver stretches for the ball. The tight end flips backward, his head strikes the frozen ground, and his neck snaps. Ben walks away unaware until the crowd falls silent and trainers rush the field. The motionless player is a young father with a wife, a toddler, and a son on the way.
Twelve years later, Lucy Cooper delivers a eulogy for her estranged father, Bud Cooper, on Winthrop Island, a small New England island off the Connecticut coast. There is no body: Bud folded his clothes on Poseidon Beach and presumably walked into Long Island Sound one week before Lucy and her seven-year-old daughter, Punkin, were due to arrive. Lucy, a widowed teacher who has lived in Paris since her husband Arnaud's murder, has returned to teach at the island school. During the service, she spots a bearded man she recognizes as Ben Ressler and is stunned, given the violence that ended his career. Her old friend Laura Peabody, whose family owns the neighboring estate Summerly, is absent.
At Windward, the decayed Cooper estate, Lucy and Punkin confront the clutter of Bud's life: maps, pirate research books, and unpaid bills, all evidence of his obsession with finding the treasure of the Dread Pirate Ned Ramsay, allegedly buried on the property. Ben appears at the door and reveals he has been living in the Summerly caretaker lodge for a year at the invitation of Laura's brother, Sedge Peabody. He and Bud became friends, and Ben found Bud's clothes on the beach. Before his death, Bud gave Ben an envelope for Lucy containing a small brass key engraved with the number 8238.
Interspersed with the present-day narrative are embedded historical chapters set in 1716. These follow Hephzibah Sykes, who lives on the island with her sister Beulah and Beulah's elderly husband, Silas Winthrop. Three men arrive by boat, one of them the pirate Ned Ramsay, gravely wounded. The ship's surgeon, Dr. Elliott, stays behind with Ramsay to recover. As Ramsay heals from the amputation of his gangrenous right arm, Elliott reveals that Ramsay served as a young officer under Captain Harte, whose cruelty provoked a mutiny Ramsay led. He showed mercy by setting Harte adrift, but Harte survived and now hunts him. Hephzibah grows closer to Ramsay as she nurses him back to health.
Lucy's financial troubles mount. A man calling himself Topher Dumont claims Bud owed the Dumont family $2.2 million, secured against the property. Sedge reveals that Ben was one of the all-time great NFL players whose career ended with the fatal hit. Lucy researches the footage and is horrified, the violence recalling how Arnaud was stabbed to death on a Paris sidewalk in a random, unsolved attack. When she tells Ben about Arnaud, he listens and says that when something is done, all one can do is live with it and make amends.
Flashbacks to the summer of 2012 trace how Lucy and Ben first fell in love. After Ben rescued Lucy from a dangerous tidal current, they began meeting secretly at dawn, their bond deepening into a hidden romance. Laura, who had an intense crush on Ben, told Lucy she trusted her above all friends. On Ben's last morning before preseason training, they made love on the beach and planned to reunite.
Through the autumn, Lucy settles into island life and begins teaching. Ben coaches the girls' basketball team. At Thanksgiving, a boy holds Punkin's head underwater; Ben rescues her. On the ride home, he reveals he put most of his football earnings into a trust for the dead player's children. That night, they discover someone entered the house while they were away. Two days before Christmas, Lucy spots a stranger watching them from the trees. Her mother identifies the mysterious key as belonging to a safe-deposit box at the family's old bank.
At the bank, Lucy learns someone already tried to access the box by impersonating her. Inside she finds only Bud's research notebooks. That evening, with Windward's furnace dead, Lucy and Punkin stay at Ben's lodge. As Lucy and Ben grow closer, he confesses he slept with Laura repeatedly the previous July, before Lucy's arrival on the island. Devastated, Lucy retreats. They barely speak for months. A fire breaks out in Windward's basement under suspicious circumstances. At Sedge's wedding, Ben pours out his heart, describing his mother's death, his fiancée leaving him for his teammate, and his exile. He declares Lucy is all he has ever wanted. She tells him she is returning to Paris.
After a crisis involving her stepfather's fraud investigation takes Lucy to London, she returns to find Laura at Summerly with an oxygen tube and a cane. Laura was diagnosed with metastatic lung cancer the previous June and chose not to pursue treatment, spending July with Ben before leaving on a solo bucket list trip and keeping her diagnosis secret. Lucy and Punkin move into Summerly. Ben sleeps in Laura's room each night to calm her terrors.
In the historical chapters, the Great Snow of 1717 devastates the island. Beulah dies in childbirth; Elliott freezes to death in a blizzard. Hephzibah and Ramsay give in to their feelings. In the spring, Captain Harte returns and captures Hephzibah at gunpoint, demanding Ramsay surrender the treasure. Ramsay brings out a chest of silver. Harte confirms the contents but raises his pistol to kill Ramsay anyway. Humility Brown, a young wet nurse Ramsay brought from the mainland, shoots Harte dead. They bury the body in the springhouse. Hephzibah tells Ramsay the silver is blood money; he dumps it down the old well, and they escape by boat. Humility Brown stays behind, eventually marrying Silas's brother Enoch and raising Beulah's baby as a Winthrop heir.
Lucy cracks Bud's laptop and discovers emails from Stephen Nye of Truro, Cape Cod. Nye claimed to possess documents locating Ramsay's treasure in the springhouse; when Bud refused to share, Nye threatened violence days before Bud's death. Lucy and Punkin find the springhouse door and discover a decomposing body inside, presumably Bud. Detective Jackson treats Ben as a person of interest, but Lucy turns over the emails pointing to Nye. At a basketball tournament, Lucy identifies the man posing as Topher Dumont as Nye. Laura discovers that Nye and his wife have been working as caretakers at a neighboring property since September, explaining the surveillance and sabotage.
During the tournament final, Nye takes Lucy and Punkin hostage. He admits to killing Bud, claiming he forced Bud to open the springhouse, found it empty, and lost control. Punkin escapes. Laura enters and knocks Nye unconscious with her oxygen canister before collapsing. Ben bursts in and tackles Nye as he lunges at Lucy with a blade. Police arrest Nye.
Laura dies in her sleep that spring. Ben kept his distance during her final weeks so she and Lucy could reconcile. After Laura's ashes are scattered at Horseshoe Bay, Ben asks Lucy whether they have a future. She tells him she is pregnant with his child. Sedge delivers Laura's final gift: Before her death, Laura sold her share of the Peabody estate for $10 million and purchased Windward, leaving it to Lucy. Ben accepts a position as athletic director at the island school, and they marry at the end of June. In the final scene, Punkin discovers loose stones in a wall, beneath which Ben finds the old well where Ramsay dumped the silver. Punkin declares her grandfather was right all along, invoking Bud's final words: "All is well."