After being resurrected, Ichabod Crane finds himself in modern-day Sleepy Hollow, where evil has awoken with him. Ichabod forms an unlikely bond with detective Abbie Mills, a young cop who has her own childhood supernatural experiences. Together, the two embark on a mission to stop evil and uncover mysteries dating back to the founding of their country.
Andy Brooks is tasked to resurrect Serilda of Abaddon, the high priestess of a dark coven, who had been captured and sentenced to death. Burned at the stake, Serilda has until the turn of the blood moon to obtain the ashes of the descendants of the men who killed her.
A rare case of suicides are going around Sleepy Hollow. One of the victims shoots himself during a police siege, but not before telling Abbie that she will be the next victim of the Sandman. With the help of a Mohawk shaman, Abbie and Ichabod undergo a ritual to enter the dream world of the Sandman, where Abbie must atone for her past actions.
When an unidentified boy is discovered in Sleepy Hollow, Ichabod and Abbie are called to the scene. After speaking with the child, they realize that a deadly plague is afoot and the duo go on a hunt to discover his home and origins, and are shocked by what they find.
When Ichabod goes missing, his wife, Katrina, contacts Abbie in a vision, forewarning of the evil to return to Sleepy Hollow by nightfall. Abbie seeks help from the mysterious Henry Parish, who holds vital clues on how he can vanquish Crane's blood tie to the Headless Horseman. Meanwhile, an encounter from Crane's past weighs heavily on him.
Ichabod, Abbie, Captain Irving, and Jenny join forces and face the Headless Horseman. While staring down his nemesis, Ichabod is shocked by game changing information about the Horseman's true motive and identity.
Captain Irving's daughter is targeted by evil forces, so he pleads for help from Crane and Mills, and looks to Washington's bible for answers. However, another frightening chapter of Jenny's past is revealed.
Ichabod and Abbie learn of a map of Purgatory that is buried with Washington's body and enlist the assistance of Henry. Meanwhile, after failing to get Abbie to hand over the map, Andy offers himself to Moloch and is transformed into a demon and attacks Ichabod and Abbie while in Washington's tomb. After understanding how dangerous the map is, Ichabod is prompted to dispose of it.
Ichabod and Abbie reach Purgatory to save Katrina in time, but it turns out that Katrina can't leave without a soul taking her place. Meanwhile, Jenny discovers a shocking secret, and she tries to reach the Witnesses in time.
To defeat the Horseman, Ichabod and Abbie seek out a patchwork man that Franklin and the Sisterhood built to oppose Moloch's servants. Meanwhile, the new sheriff arrests Jenny and Frank explains that demons killed his supposed murder victims.
Ichabod and Abbie discover that Henry is trying to spread a curse of violence, unleashing the darkness in individuals so that they kill. Meanwhile, Jenny discovers who was responsible for her mother's imprisonment at Terrytown, and Frank learns the truth about his lawyer.
Corbin's son Joe returns from overseas after receiving an honorable discharge after his platoon is wiped out in a bizarre attack. Ichabod and Abbie soon realize that something is wrong with him. Meanwhile, Henry tells Irving that there is a way for him to free his soul, but it has a cost that Irving may not want to pay.
Henry brings in a doctor to monitor Katrina's condition after her sudden illness. She manages to escape and Ichabod finds her, and they realize that Moloch has a new plan to manifest on Earth. To stop him, Ichabod reaches out to Henry to use his powers to save his mother.
Ichabod and Abbie discover the existence of the Sword of Methuselah, the only weapon capable of killing Moloch. They race to find it, only to discover that Henry has learned of the weapon's existence and sent the Horseman of Death to get it first.
Nick's godmother, the woman who raised him after his parents died, asks for his helping stealing a mystic artifact. He reluctantly agrees, putting him at odds with Abbie, Ichabod, and Jenny. Meanwhile, Irving is cleared of the charges against him but Cynthia still has concerns.
Solomon Kent, a warlock who set off the Salem Witch Trials to protect himself, seeks out a Grimoire that will give him the power to undo the mistake in his past that turned him into a warlock. Meanwhile, Irving approaches Abbie, while Henry contemplates his past and decides on his future.