The Sheriff goes to the hospital after Isaac and Braeden are brought in in critical condition. He wants to talk to Braeden, but Melissa tells him she's under heavy sedation. He asks her to call him when she's awake. He next ends up at the school after a flock of birds attack Jennifer Blake's class. He asks Chris if he's ever seen anything like this since Chris is "a hunter," but Chris says no. He goes to talk to Deaton about it and learns that the animals in the clinic are also acting strange, killing themselves in their cages.
The Sheriff goes to the school to pull Stiles out of class because he was the last person to see Heather before she disappeared. Stiles doesn't have anything to tell him, though. The next day, he finds Stiles and Scott asleep in Stiles's room with books and papers everywhere. He wakes them up so they can go to school. Stiles realizes that his dad worked on the bank robbery case they'd been researching and decides to ask him about it. The Sheriff provides him with all kinds of details and maps about the robbery.
Caitlin and Emily are in the woods on a date when Emily disappears. Caitlin goes to the police and explains what she saw, though the Sheriff doesn't really believe her because she admits to being on ecstasy. The next day, they find Emily, killed using the threefold death.
When the cross-country team is out running they find Kyle, who had gone missing from the animal clinic the night before. He's dead, and the Sheriff tries to get everyone back so they don't contaminate the crime scene. He takes Kyle's girlfriend, Ashley, to the principal's office to interview her. As she leaves he hears Stiles ask her if Kyle was a virgin and then yells at him for butting in and being insensitive.
After Dr. Hilyard's car shows up at the hospital without Dr. Hilyard, the Sheriff comes over to take a statement about the two doctors that are now missing. The next day, it's unclear whether Scott calls the Sheriff to tell him that Deaton is going to go missing or the Sheriff finds out some other way. Regardless, they meet up at the Animal Clinic and Scott tells him everything he can without revealing the supernatural. They find Dr. Hilyard's body later that day, and as the Sheriff escorts it to the morgue, Melissa pulls him aside to explain how the healers are dying without being strangled. She shows him the deep wounds on their wrists and says they are being hung up until they asphxiate from their own body weight. He does some more police work on finding Deaton and ends up going to the Beacon Hills First National Bank. He shoots the rope that's holding Deaton to the ceiling and explains that it was a celtic symbol which he saw in Deaton's office that led him there because it looked like the bank logo.
The Sheriff appears in the story that Peter and Gerard are telling. He was a deputy during the time that Paige was killed. He was called to the hospital because Ennis was starting a fight with the nurses over his right to see his beta's body. Stilinski stands up to Ennis despite his superior size and informs him that the young man's death launched a murder investigation.
After Tara is found murdered at the school, the Sheriff comes in with FBI to investigate. Stiles tries to talk to him about the murders being ritual sacrifices, but he doesn't want to hear it. When more teachers start being taken, Stiles decides to tell his dad the truth. He sets up a chessboard and labels the different pieces so he can explain who are Werewolf, hunters, and Druid. The Sheriff tries to follow it, although he screws some of it up, but he fundamentally doesn't believe anything Stiles is saying. Cora is about to shift in front of him to prove it, but she passes out instead. The Sheriff and Stiles takes her to the hospital. Stiles tries again to convince him that he's right, but the Sheriff yells at him that he's been listening to everything he's been saying but he has to follow the evidence. Stiles realizes that his dad doesn't believe him and claims that his mom would have. It's a low blow. On his way out he asks Melissa to look up a particular medical file on a girl he brought in who was slashed in the face. She's able to find it and tells him that while the girl was in the hospital birds kept killing themselves near her window. He heads to the school, where all the teachers are gathered. Somehow, the Sheriff isn't at the recital but is instead close enough that when Lydia screams, he's able to find her. He stops Jennifer from killing her and reveals that he knows she was the one he found in the woods. She approaches him, healing the bullet holes he puts into her, and then kisses him. The Sheriff is kidnapped as the first guardian sacrifice.
The Sheriff is tied up under the nemeton. When Melissa wakes up tied to a post across from hhim, he asks if she's okay and reveals their location.
Chris wakes up in the nemeton with the Sheriff and Melissa and laughs because he knows where they are. As he starts to search for his weapons, the Sheriff informs him the Jennifer took them all. He watches Chris struggle with the ropes and they talk about whether being tied up is a normal part of being a hunter. The Sheriff believes a little bit more about the supernatural now. Chris tells him that they met once before, many years ago, and the Sheriff knew something hinky was going on but wasn't ready to believe in the supernatural then. Stilinski admits that this is true. The night his wife died, he was at the scene of a car accident with a dying girl. The girl told him that he had to leave if he wanted to see "her" again, and he knew the girl was talking about his wife, but he didnt' believe that she could know something like that. The girl in the car died, and by the time the Sheriff got to the hospital, Claudia was already dead.
The parents continue to wait to be rescued. Melissa asks if either of them have an itch they can't scratch, and the Sheriff replies that he didn't before but he does now. She asks if Jennifer is really going to slash their throats, and the Sheriff says that Jennifer will strangle them and then slash their throats. A storm starts kicking up as Allison and Isaac get closer to finding them, and the root cellar starts to collapse. Isaac and Allison jump into the cellar and release their bonds, but the stairs fall down before any of them can get out. Isaac braces himself under the ceiling beam to keep the cellar from crushing them entirely. When Isaac can no longer hold the beam on his own, everyone else starts to join in, but just then Stiles appears with a bat, that he uses to prop up the beam. The Sheriff jokes about how much more he likes metal bats and then hugs his son.
It's unclear how long this has been going on, but the Sheriff runs into Stiles's room when he hears him screaming from a nightmare. He holds him while Stiles wakes up, fighting and crying, and tries to soothe the terrors away. The next morning, Stiles is acting strangely and his father asks if he's okay, but Stiles doesn't want to talk about it. Instead, he asks the Sheriff about a box of files he's carrying from the station. The Sheriff has been going through all his old cases looking for new supernatural explanations. He's marked up all the full moons on the wall and has been plotting the unsolved cases against them. Stiles comes to see him later and takes note of his new investigations. He now has a kanima pile. But the case that stands out for him is the Tate car crash. 8 years ago his first duty as sheriff was to tell Henry Tate that his family had died and daughter gone missing. The crash occurred on a full moon, which makes it suspicious. Stiles then asks where all these case files are going and the Sheriff reveals that Rafael McCall is trying to impeach him.
Later, he finds Scott and Stiles at the Animal Clinic because he wants Scott's help in looking for Malia Tate, the girl who went missing 9 years ago. They all go to Henry Tate's house, and while the Sheriff talks with him, Scott and Stiles looking for something to get a scent off of. Stilinski asks Henry Tate questions with the idea that maybe his family was murdered. Henry Tate doesn't want to entertain this notion because it's taken him this long to get used to the idea that it was an accident. He makes the Sheriff leave, and outside Scott and Stiles report that they couldn't find anything. The Sheriff apologizes, not sure what he was thinking getting them involved in this or reopening old wounds.
The Sheriff gets a call from Scott and Stiles reporting that they found Malia's den. The Sheriff asks if they're sure it was Malia, because it sounds like all they know is that they have a shapeshifting coyote on their hands. Scott surmises that she could have shifted on the full moon, which caused the accident, and then she got stuck. The Sheriff thinks this is a pretty tall tale and tells them to keep it under wraps. Just then Agent McCall shows up with Henry Tate, who confirms that the clothes they found in the den were his daughter's. Stilinski is angry that McCall thought it was a good idea to bring Tate there. McCall thinks they'll find a body soon, which will give Tate closure. The police get called to the school the next day because a coyote attacked Kira on school grounds. Stiles explains to his dad that they're sure it's Malia, so he can't just put the coyote down if they find it. Stiles argues that Scott is sure it's her. When Scott shows that he can hear their whispered conversation from down the hall, it seems to remind the Sheriff that the supernatural is real.
Henry Tate shows up at the school, and the Sheriff has to get him to back down. Tate came into the school wearing a gun. Even though he has a permit, guns are not allowed on school grounds. Tate leaves but only after imploring the Sheriff to kill the coyote. Later, the Sheriff goes out to Henry Tate's house and slams a steel jaw trap down in front of him. He demands to know how many traps Tate has set, and then sees an entire room full of empty boxes. A kid could die in one of these traps, so the Sheriff says they're finding and disarming everyone of them. While they're fighting, they notice a tear in the screen door. The coyote has been inside the house. Tate grabs his gun and finds the coyote outside with the doll Stiles took from the crash site. The Sheriff orders his people to clear the woods. After Scott forces Malia to shift back into a human, the Sheriff takes her to her father.
Agent McCall brings William Barrow to Beacon Hills Hospital because he needs surgery and no one else will take him. The Sheriff tries to refuse, but there's nothing he can really do. When Barrow's surgery goes wrong, Agent McCall and the Sheriff rush into the room, but he's already gone. Melissa tells him that live flies came out of Barrow's tumor, which is basically impossible. She also says that Barrow was trying to kill kids with glowing eyes. The Sheriff gets a call that the ambulance Barrow stole was spotted near the high school, and he heads to the school. He tells Stiles about the kids with glowing eyes, and Stiles spreads the information around. The police search the school but don't find anything. As they're leaving, Stiles asks his father not to give up the search. He tells him that Lydia knows Barrow is still there. This is how the Sheriff learns that Lydia is a banshee. He can't even believe what he's hearing. He leaves a few deputies on campus and locks the school down until 3.
Scott, Kira, Stiles, and Lydia are in the Sheriff's office being questioned by Agent McCall. Stiles dodges out of most of the questions, and the Sheriff tries not to be amused at how annoyed McCall gets. He claims that he hasn't trusted anything Stiles has said since he started talking, which Stiles seems to take to heart.
Lydia makes Scott tell the Sheriff that Stiles has gone missing. At the station, the Sheriff puts out an APB on Stiles's Jeep, which is quickly found in the hospital parking lot. He also has a deputy get a list of industrial buildings with basements Stiles would be able to sleepwalk into. Then he pulls Scott and Isaac aside and asks if there's anything they need to tell him that they can't say in front of other people. They reveal that Lydia knows he's missing through her powers and she's working on a location. They all head to the hospital, and Melissa takes the Sheriff to the basement to check there. When Lydia tells them that she's sure Stiles is at Eichen House, they all head over. They go into the basement, but he's obviously not there. Lydia is confused, and the Sheriff loses his temper. Melissa and Agent McCall find him instead, and they all head back to the hospital. While Stiles is resting, Melissa tries to broach the subject of his symptoms, but the Sheriff already knows. He's been keeping a list and he knows that it matches Claudia's symptoms. He thinks they need to run some tests. During Stiles's MRI, Melissa stands right next to him to watch. The results are everything they feared. When the power to the hospital goes out, they lose track of Stiles in the chaos.
Everyone is searching for Stiles, so the Sheriff sits at work. He signs for some packages and stares at the text message Stiles left him telling him not to worry. Agent McCall asks him if he's ever had problems with the yakuza, specifically Katashi, which the Sheriff finds a confusing line of questioning. He gets a call about a bomb threat at the school and heads over there with Parrish. Parrish is trained in bomb detection and defusion, so he goes in. What he finds is the Sheriff's name plate from his office. They realize that there is a bomb but it isn't at the school. They call the station to have it evacuated, but there isn't time for everyone to get out. When the Sheriff gets back, he tries to help the wounded.
Stiles has asked to be put in Eichen House while the Sheriff goes to LA to have a specialist look at his brain scan. Stilinski is clearly unhappy about doing this to his son, but it's what Stiles wants. They go to check in and are told that Stiles will not be able to make any calls for 72 hours. The Sheriff realizes that they forgot Stiles's pillow and is ready to call this whole thing off because of it, but Stiles convinces him otherwise. He leaves Stiles there and heads to LA the next day.
With no evidence tying them to Katashi's murder, Chris and Derek are released from jail. Deputy Jordan Parrish doesn't want to give Chris his electrified baton back because it's way above the legal limit. The Sheriff takes control of the situation and asks Chris and Derek to come talk to him in his office. He shows them the scan from Stiles and the scan from Claudia. They are exact match, which isn't possible. It's a trick from the nogitsune to make Stiles lose hope. He asks Chris and Derek if they will help him catch the nogitsune. They agree and head to the Argents' apartment where Allison has assembled all their non-lethal weapons. They try to decide what to do. Breaking up and going to all Stiles's regular haunts is the same thing they did before and didn't work. They don't have a better plan, though. Chris and Derek go to Eichen House with Allison and the Sheriff go to the hospital.
While they're in the elevator, the Sheriff admits that he doesn't know how Allison stays so calm and fearless. She tells him that she's scared all the time and starts to cry. He pulls her into a hug and says that she sounds like a cop. While she collects herself, his phone goes off with a warning from his new home security system. He checks and sees video of the nogitsune waving at him from Stiles's room. They all head there and find the chessboard rearranged. Derek is now the king one move from checkmate. Chris thinks this is a threat. Allison suggests that it could mean they'll find him at Derek's loft. The Sheriff believes that they need to come up with a new punch line to whatever joke the nogitsune is telling. Everyone agrees to hear him out, and then they all head to the loft.
The Sheriff approaches the nogitsune first and asks him to let him cuff him. He allows it, but then quickly breaks the cuffs off. Everyone else tries their luck, until Chris draws a gun on him. The Sheriff draws a gun on Chris, ordering him to put it down. The nogitsune enjoys their anger and bides his time waiting for sunset. Once the sun goes down, the Oni appear, and the nogitsune takes shelter behind Chris, the Sheriff, Derek, and Allison and then disappears entirely. The Sheriff goes back to work, where Agent McCall informs him that he has to come to a hearing or be fired. The Sheriff brings his badge and gun with him in case he has to turn them in. At the hearing, the reviewer has two stacks of files, one for successes and one for failures. It's clear which is which. The Sheriff has no patience for any of this and doesn't want to make a statement on his own behalf. Luckily for him, Agent McCall steps in and does it for him. When it's over, he thanks McCall for saving his job. McCall admits that not even Sherlock Holmes could figure out all the weird stuff in Beacon Hills.
No one has been able to tell the Sheriff that Stiles has been found and separated from the nogitsune, so he just sits in his office long after he should have gone home, thinking and waiting for news. Parrish tells him to go home, but he won't. He asks Parrish how he ended up in Beacon Hills, and Parrish just says he felt drawn there. Parrish tries again to send the Sheriff home, and this time he decides to listen. While he's looking for his keys, Scott and Stiles arrive. The Sheriff checks with Scott whether this is actually his son, and when Scott nods, the Sheriff hugs Stiles. They inform him that now Lydia is missing, so the Sheriff puts an APB out on her car. Stiles also suggests asking Meredith Walker from Eichen House about Lydia, because she seemed to hear things that no one else could hear also. Parrish finds out that Meredith is still at Eichen House, although she's been moved to the ward for violent people. Brunski leads the Sheriff toward Meredith's cell. They find an orderly with a needle in his back and Meredith missing. The Sheriff helps them search Eichen House for her.
After Allison's death, Agent McCall takes everyone's statements in the Sheriff's office. Stilinski pats Isaac on the shoulder whie he repeats that it all happened so fast. After they're gone, he asks Parrish to help him keep a lid on it so the media doesn't have a field day with it. Parrish asks if he'd like a detail placed outside his house. The Sheriff agrees. Oni suddenly appear in the station and Parrish draws his gun and fires. They start fighting Oni. The Sheriff gets a shotgun, which helps a little, but he ends up getting cut anyway. Parrish gets cut also, and then the Oni vanish. Black smokes comes out of their wounds, and the Sheriff isn't sure that the Oni left because they were letting them live. The cuts heal when the nogitsune and the Oni are destroyed.