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.
A young girl mysteriously goes missing and Abbie goes on the case to search for her with the help of Ichabod. The search leads to a major clue, implying that they're dealing with something supernatural.
After having something put in her by Jeremy, Katrina seeks help from both Ichabod and Abbie who eventually discover that Katrina is pregnant with a demon, Moloch. Ichabod goes by all means to prevent the birth or else she could die.