Ichabod Crane and the Headless Horseman awaken in 2013 Sleepy Hollow, NY. Lt. Abbie Mills brings Crane along with her to hunt the Horseman. The local DA and law enforcement believe Crane to be a madman who claims to be from Colonial America and he may be the killer of the former sheriff, as nobody could believe a headless horseman possibility. The Headless Horseman is believed by Crane to be The Horseman of the Apocalypse: DEATH. Meanwhile, there are secrets in Sleepy Hollow Abbie and Crane must uncover to find out why the Horseman remains in Sleepy Hollow.
The Demon who killed Deputy Andy Brooks brings him back to life to aid in the resurrection of Serilda of Abaddon, the high priestess of the dark coven, who had been captured (with the help of Ichabod's wife Katrina) and 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, and Abbie and Ichabod confront the witch in the subterranean tunnels underneath the sheriff's station as she attempts to complete her revival ritual. Abbie has a vision of Sheriff August Corbin, who tells her not to be afraid of "49".
A psychoanalyst who had treated Abbie's sister Jennifer throws herself off a building, and her eyes are found to be full of sand. Mr Gillespie, who also saw the demon encountered by the Mills sisters ten years earlier, shoots himself during a police siege, but not before telling Abbie that she will be the next victim if she falls asleep. With the help of a Mohawk "shaman"/used car salesman, Abbie and Ichabod undergo a ritual to enter the dream world of the Sandman, and Abbie must atone for her past actions.
When Ichabod Crane goes missing, his wife, Katrina, appears to Lt. Abbie Mills in a vision warning her that the Headless Horseman will return to Sleepy Hollow by nightfall. A frantic Abbie seeks help from the mysterious Henry Parrish (guest star John Noble), who holds vital clues about how Crane can vanquish his dangerous blood tie to Headless. Meanwhile, an encounter from Crane's past weighs heavily on him, and details about his first encounter with Katrina are revealed.