When Lydia goes missing from the hospital, the Sheriff is called in to begin a search. Stiles rattles off all of Lydia's relevant details, and then the Sheriff sends him home.
After Kate's body is desecrated in the graveyard, the Sheriff discovers that Isaac is being abused by his father. He asks Issac about his black eye and knows that he's lying when he said he got it at school, but he has no evidence to that effect.
Later that day, the Sheriff is at Kate Argent's funeral, attempting to control the crowd. He catches Scott and Stiles spying on the funeral and brings them back to his police car. While there, they get a call for a 415A in an ambulance on Route 5 and Post. The Sheriff turns around to talk to the boys, but they have both fled the car, so he heads to the scene. Stiles meets up with his father there, and Lydia comes stumbling out of the woods, naked. The Sheriff gives her his coat since Stiles is struck dumb.
After Isaac's father is killed, the Sheriff shows up at the school to arrest Isaac and question Jackson because Jackson lives across the street. Jackson confirms that Isaac's dad was beating the crap out of him, and the Sheriff is appalled that Jackson never felt the need to tell anyone about it. “…it’s funny that the kids getting beaten up are always the ones that least deserve it.” As he leaves the office, he ignores Stiles who is hiding behind a magazine.
The police take Isaac into custody and put him in a holding cell in the station. The next time the Sheriff enters the station, the holding cell is busted open, a hunter dressed as a deputy is unconscious on the floor, and Stiles is standing in the middle of the room.
The next major crime the Sheriff is called to is the death of Tucker Cornish at the Armor Tire, where Stiles was getting his Jeep fixed. He's convinced that Stiles isn't giving him the full story of what happened, but Stiles sticks to his guns and eventually the Sheriff lets him leave.
After being abducted and tested with kanima vemon, Jackson is sent back to Sheriff Stilinski to recant his testimony that Isaac was fighting with his father. The Sheriff asks him if he saw a fight, and Jackson tells him, "Not exactly." The Sheriff explains that in law enforcement there's a very large divide between "not exactly" and "no." "Like if Not Exactly were sitting in this chair, then No would be somewhere in the middle of the Pacific Ocean drowning next to my career."
Without the testimony, Isaac is no longer a wanted man.
When the kanima attacks Danny at the Jungle, the Sheriff and EMTs show up to treat those who are paralyzed. Just as Stiles and Scott are about to drive away with Jackson in the car, the Sheriff drives up and blocks in his car.
Stiles gets out to talk to his dad while Scott tries to keep Jackson quiet. Stiles tells his dad that they were out clubbing. "Not exactly your type of club," the Sheriff says. "Well, dad, there's a conversation we need to have." "You're not gay." Stiles is offended. "I could be!" "Not dressed like that." Stiles doesn't see what's wrong with his clothes, and his dad tries to get closer to the Jeep. Stiles stops him and his dad tells him that it's the second crime scene that he just happened to be at and he's been fed so many lies he's not sure he knows his own kid. Stiles tells him "the truth" which he says is that they were there with Danny who just broke up with his boyfriend. They were trying to take him out and get his mind off of it. The Sheriff tells him that they're good friends and lets Stiles go.
The following day, Mr. Whittemore goes to see the Sheriff because he knows something is wrong with his son. He got a text saying, "Stayed at a friend's house last night. Everything fine. Love you." Jackson hasn't been able to tell his parents that he loves them since they told him he was adopted 11 years ago, so his father knows something is wrong.
Jackson escapes, and Scott and Stiles go down to the sheriff station to finally tell Sheriff Stilinski the truth. Instead, they find Mr. Whittemore, Jackson, and the Sheriff already having a conversation. The Sheriff informs them that Jackson's father is a lawyer, just in case it wasn't clear that they were in trouble.
Scott and Stiles are brought into an interrogation room where the Sheriff reads out the restrictions of the restraining order Jackson's father has taken out against them. They cannot go within 50 feet of Jackson, speak to him, approach him, or assault him physically or psychologically. Melissa McCall and David Whittemore are in the room witnessing. The Sheriff drops the order to the table, and Stiles asks him what about school. They can attend classes while attempting to maintain a 50 foot distance. Stiles asks what happens if they both have to use the bathroom and there are only two stalls and they're right next to each other, and the Sheriff glares at him while David Whittemore gets incensed at Stiles making a joke.
The Sheriff takes Stiles out into the hallway and reminds him that he's lucky Jackson isn't pressing charges. Stiles explains that it was all a joke and he didn't think it would be taken that seriously. The Sheriff asks him how he's supposed to interpret the humor of a stolen prison transport van. Stiles exclaims that they filled the tank.
Mr. Whittemore continues to yell at him for Stiles's disrespectful behavior.
Later in the week, Stiles and the Sheriff are having dinner in his office. Sheriff Stilinski takes a bite of dinner and makes a face. "Oh what the hell is this?" "Veggie burger!" Stiles chimes. They're having a healthy dinner, and Stiles holds up his salad. The Sheriff opens what he expects to be fries and finds celery and carrots. "Why are you trying to ruin my life?" "I'm trying to extend your life." Stiles asks his dad to tell him what he found, and the Sheriff says he's not sharing confidential information with a teenager. Stiles notices a large case board on the wall behind him and asks if that's it. Stiles takes a closer look, and his dad tells him to avert his eyes. Eventually he relents and tells Stiles that he did find something in common with all three kanima murders. "One's an incident, two's a coincidence--" "Three's a pattern," Stiles finishes.
The mechanic, Sean, and Jessica were all 24. The only one that didn't fit the pattern was Mr. Lahey. The Sheriff thought that might mean it was not connected, or that the ages were a coincidence. But then he found that Isaac had an older brother named Camden. If Camden were alive, he'd be 24, but he died in combat.
Stiles asks his father if thought of same age meaning same high school class. He hadn't and says that he only got Lahey's file two hours ago. Stiles is incensed. They go with the same class idea and grab Beacon Hills High School yearbooks. They were all class of 2006. The Sheriff suggests that they could have had the same classes together. Then he flips open a file and sees a photo of Mr. Harris and says they could have had the same teacher. He tells Stiles to put faces to everyone who was in Harris's 2006 Chemistry class. If the killer isn't done, then someone in that class could be next.
On Friday, Sheriff Stilinski gets home just as Stiles is running out. Stiles notices his father's mood and asks him what's wrong. Then he asks him where his gun is. "I left it at the station along with my badge." Stiles is stunned. His father tells him that they'll talk about it later. Stiles tries to talk about it now, but his dad tells him not to worry. Stiles insists. "It was decided that the son of the police chief stealing police property and having a restraining order filed against him by one of the town's most respected attorneys did not reflect well on the county."
Stiles realizes that he got his dad fired. The Sheriff tries to tell him that it's a temporary leave of absence, but they didn't say that when they let him go. He again tells Stiles that they're going to be fine. Stiles asks him why he isn't angry at him. "I don't know. Maybe I just don't want to feel any worse than I already do by having to yell at my son."
Despite being fired, Sheriff Stilinski shows up at the rave where someone has been murdered. David asks him if he thinks it's a good idea being there. The Sheriff responds that he just wanted to know her name. David tells him it was Kara. The Sheriff checks his list of names, and hers isn't on it.
The following week, The Sheriff walks by Stiles's room and stops to ask him what he's up to. Stiles absently answers homework. The Sheriff comes back to the door when he remembers that it's spring break. He comes into the room and closes the yearbook. The Sheriff tells him that Mr. Harris was brought in for questioning and they're working on a warrant to arrest him for the murders. Stiles asks what proof they have, and his dad says they have tire tracks near Sean's trailer that match Harris's car. Someone also saw the car outside the hospital where Jessica was killed. He tells Stiles about the bumper sticker, and Stiles tells him that he saw the car outside the rave. Stiles will have to give a statement, since that makes him a witness.
Stiles is concerned that Kara wasn't in Harris's class and that Mr. Lahey doesn't fit the pattern, but his father says that being at the sites of three murders is damning evidence. Stiles still doesn't feel it's enough evidence and goes back to looking through the yearbook. His dad thought he hated Mr. Harris. "I don't hate him. He hates me," Stiles says, but he still feels there's something missing. The Sheriff tells him that he doesn't have to solve the case for him, but Stiles thinks that he does. Just then, the Sheriff looks down at the page Stiles has stopped on. It's a photo of the swim team. All of the victims were on the team, and Mr. Lahey was the coach.
The Sheriff appears as a hallucination to Stiles during Lydia's birthday party thanks to wolfsbane punch. "Why am I wearing black? What are you, an idiot? I just came from a funeral, you know people wear black at funerals." He's yelling at some kid at the party and then shoves the kid away. Stiles is struck dumb. The Sheriff then turns to him. "It's you. It's all you. You know every day I saw her lying in that hospital slowly dying. I thought how the hell am I supposed to raise this stupid kid on my own. This hyperactive little bastard who keeps ruining my life. It's all you. It's you, Stiles. You killed your mother, you hear me? You killed her. And now you're killing me." The Sheriff then hurls his whiskey bottle at Stiles, and the hallucination ends before it can hit.
Once Scott sees that Matt Daehler is controlling the kanima, he and Stiles try to convince the Sheriff that Matt is the killer he's been looking for. The Sheriff doesn't believe that Matt's the killer. Stiles argues that everyone knows how the police attempt to track down murderers, so all Matt had to do was track down which class all his victims had in common. His dad points out that Kara wasn't in Harris's class, which they both already knew. Scott confirms that they know it's Matt without being able to say why. Stiles says that Matt stole Harris's car and purposefully left evidence to set him up. The Sheriff asks them for motive.
"Isn't it obvious! Our swim team sucks! They haven't won in like six years. Okay, we don't have a motive yet." But then neither does Harris. The Sheriff asks the boys what they'd like him to do. Scott says they need to look at the evidence, and the Sheriff tells him that it's in the station where he no longer works. "Trust me, they'll let you in," Stiles tells him. His dad is incredulous that he would suggest he is trustworthy, so Stiles points over his shoulder. "Trust Scott?" The Sheriff agrees to trust Scott.
They head to the sheriff station at 2am. Stiles tells Scott that they need to start by looking at the hospital murder, which is the only one not committed by the kanima. An officer lets the Sheriff into the office. They start looking through the hospital security camera footage. Scott thinks he sees something and asks the Sheriff to scroll back. Stiles recognizes the back of Matt's head because he sits behind him in history. "Look at his jacket. How many people do you know who wear black leather jackets?" "Millions. Literally." Scott asks him to scroll forward, and they see Matt talking to Melissa McCall.
Scott calls him mom, and they ask her if she remembers Matt. She tells him that she talks to a lot of people, so they send her Matt's yearbook photo. She says that she remembers Matt because he was tracking mud in the hall. The Sheriff pulls out a file. They have footprints from the trailer site, and if they match that puts Matt at the trailer, the hospital, and the rave. The Sheriff corrects him. There's a credit card receipt for an oil change signed by Matt at the Armor Tire a couple of hours before Stiles arrived. The Sheriff says that four is enough for a warrant. He has Scott call his mom back and ask her to come to the station.
Scott says that his mom is on her way, and then the Sheriff sees Matt leading Stiles back in at gun point. The Sheriff tells Matt that there's a solution here that doesn't involve a gun, and Matt replies that he's more correct than he knows. The Sheriff tries telling him that he doesn't want to hurt people, but Matt actually does. The three of them weren't on his list, but he can add them if Scott keeps doing things like trying to dial his cell phone in his pocket. Matt makes them all put their phones on the desk. Then he has Stiles cuff the Sheriff onto one of the benches by the cells.
Eventually, he is able to pull the bar that he's been cuffed to out of the wall, but Matt pistolwhips him and knocks him out before he can do anything. By the time he wakes up, Matt is dead and floating in the river.
Because Matt was identified as the killer and they were, presumably, able to salvage some of the evidence the Sheriff had put together, he was given his job back.
The night of the championship game, the Sheriff is in the stands, sitting next to Melissa. He groans wondering why Stiles is running onto the field. "Because he's on the team?" Melissa replies. And the Sheriff realizes that Stiles is actually going to play. He's so excited he gets up and cheers just at that.
Stiles gets the ball a few times but gets creamed by the other team each time. Once, he misses catching the ball and it hits his helmet instead. The Sheriff, Melissa, and Lydia all look mortified.
Eventually, the ball rolls to Stiles's feet. None of the other players know where it is, so Stiles picks it up and starts running. He stops in front of the goal, terrified, and doesn't shoot he ball until Lydia shouts at him. He scores! Everyone cheers!
At the end of the game, the lights on the field go out. When they come back up, Jackson is lying dead on the field. The Sheriff breaks into the circle around Jackson and looks around for Stiles. "Where the hell is my son?"
Sheriff Stilinski tells Scott and Isaac that he's going to meet with the ME and see if he can find out what happened to Jackson. He's also got an APB out on Stiles. The Jeep is still in the parking lot, but the Sheriff doesn't know what that means. He tries to keep his emotions under control as he asks the boys to contact him if they hear from Stiles. Scott promises that they'll find him.
The Sheriff goes back home and is standing in his son's room reporting that he's not finding any clues. Stiles walks into his room, beaten and bruised, to find his dad asking wondering out loud where he is. "Right here," Stiles says. His dad rushes forward to examine his face, and Stiles tries to tell him that he's okay. The Sheriff demands to know who did it. Stiles lies and tells him it was just some kids from the other team. His dad asks for descriptions, but Stiles tries to calm him down by insisting that it's not that bad. The Sheriff turns his fear into anger and says that he will "personally go down there and pistol whip these little bastards." Stiles yells at his father to calm him down, and they hug each other.
Later that evening, Lydia comes to see Stiles. After she leaves, Stiles sits in his room alone, checking his phone. His dad comes in and asks him if there's anything romantic brewing with Lydia. Stiles tells him that she's in love with someone else. The Sheriff comes and sits next to his son, concerned that everything that's happened with the beating and Jackson has got him shaken, but he reminds him to be happy about the game. Stiles doesn't take much comfort in this, but his dad presses the point. "You weren't just the MVP of the game. You were a hero." Stiles denies that he's a hero.