Derek appears at the hospital to save Isaac from Ennis and the alpha pack, only he ends up also saving Scott as well, who is no match for Ennis. Together, they take Isaac from the hospital and go to the Hale House so Derek can get something, possibly wolfsbane, that will help Isaac start to heal. Scott asks him about what's going on, but Derek dismisses his concern and tells him to go back to his life, not wanting anything to do with Scott after his betrayal in 2x12 - Master Plan. Scott then asks Derek to help him make his tattoo permanent in exchange for his attempt to save Isaac, and Derek agrees. With his alpha vision, he's able to see the tattoo and asks Scott for an explanation for the symbol. Satisfied with the answer, he makes Stiles help hold Scott down while he burns him with a blow torch.
As Scott and Stiles are about to leave, Scott realizes the door to the Hale House has been painted. Derek tells him to leave it alone, but Scott scratches off the paint, revealing the alpha pack symbol. Derek explains about the pack and how he's been searching for Boyd and Erica for months. The exchange of looks between Derek and Stiles implies that Stiles has been helping over the summer, though nothing is stated.
Isaac recovers from his injuries, but he can't remember where he found Boyd and Erica. Derek decides to ask Peter for help. Neither of them are too happy about it, but Derek has never done a mind meld with anyone before and doesn't want to hurt Isaac by trying. They learn that Erica and Boyd are going to die the following night, on the full moon. Scott calls Derek with news from Lydia and Allison, and they all meet at the school. Derek isn't impressed by the symbol the girls have burned into their arms, and he doesn't trust any of them. Stiles tries to placate him by pointing out that no one got killed, only Allison points out that her mother did. Derek tries to get Scott to tell Allison what really happened with Victoria.
Derek, Scott, Stiles, and Isaac go to Deaton to try to find a way to jog Isaac's memory. He's submerged in an ice bath almost to the point of death. Isaac fights the memories, but Derek pressed him to keep going and eventually Isaac reveals he found them in a bank vault. He also tells them that Erica is dead. Derek refuses to believe that but decide they need to break them out ASAP. The following night, Stiles, Scott, Derek, and Peter meet at the loft to plan the break-in. Derek is sure that he can punch through the wall, but he humors Stiles when Stiles tries to show him that that's crazy. Derek asks Scott for his help, and the two of them head off. Only after they've broken into the vault do they learn that Boyd and the other Werewolf inside haven't shifted in months and so will be extra rabid. Derek discovers that the other Werewolf is his sister, Cora. He and Scott try to fight them off while locked in the vault, but Allison breaks the mountain ash seal holding them all inside, to Derek's dismay. He yells at her for letting them free and insists again that Scott tell Allison what happened with her mother so she'll stop holding a grudge against him.
Derek and Scott immediately head out after Boyd and Cora to try to keep them from killing anyone. They just barely manage it, and when they learn that a boy near a pool has been killed, Scott assumes Boyd and Cora are responsible. Derek doesn't understand how they could have gotten across town so quickly, but he accedes that they might have to kill them to stop them. Scott asks Chris Argent for help, although Derek isn't happy about it. Peter shows up to tell him that he's making terrible choices and doing just what Deucalion wants if he kills them.
They round Boyd and Cora up into the school and lock them in the boiler room. Only then do they realize there's another person in the boiler room. Derek goes in, ready to die if that's what it takes to keep the third person safe. He lets Boyd and Cora claw at him while holding them apart until the sun rises and they pass out. Then he finds Jennifer cowering in the supply cage and offers her his hand to lead her out of there.
Derek returns to the school to check on Jennifer. She's afraid of him, but they flirt a little and he leaves with telling her his name. He goes back to the loft and finds Cora working out. They banter, but then the alphas break into the loft and attack. Kali shoves a pole through Derek's back and holds him while Deucalion comes in to have a chat. He explains that he wants Derek to kill his pack and join the alphas. After Duke rants, Kali takes the pole out of Derek, and they leave.
Later, Derek tells Isaac that he needs to leave the loft. Isaac doesn't want to go, so Derek throws a glass at him, mimicking the abusive way Isaac's father used to treat him. It works, and Isaac leaves.
Through flashback it's shown that Derek, Peter, and Cora are planning to attack Deucalion. Scott tried to head off that attack by going to meet with Deucalion on his own. However, Derek's Pack followed him to the meeting place, an abandoned mall, and a fight ensued. Derek fought with Ennis, and they both fell from an upper level when Scott clawed Ennis's leg. Scott thought Derek was dead. Apparently no one checked if he was really dead and just left the mall.
In present time, Derek shows up at the high school parking lot at Jennifer's car. He's covered in blood and smears some on her window as he collapses.
Jennifer brings Derek back to his loft, even though she thinks she should take him to a hospital. They collapse just inside the door. She struggles but eventually gets him into bed and checks his wounds. Derek is barely conscious. A few hours pass and Derek regains consciousness and sits up. Derek wants to call his pack and tell them that he's okay, but Jennifer thinks he should take advantage of his faked death. He tries to tell her to leave because everyone around him gets hurt, She doesn't want to go and moves in to kiss him. They sink back onto the bed and have sex. Derek's wounds heal while doing so.
Derek fell asleep reading, but he wakes up when the proximity alarm in the loft goes off. Cora asks him what it means, and they realize that the alpha pack put their symbolon the window. He says it means they're coming for him tonight. Boyd and Isaac skip school in order to help Derek protect himself from the alphas. Their plan is to flood the loft and electrify the water on the floor. They sit on boards just above the water and wait. It seems like a good plan until the power in the building is cut.
Kali shows up at the loft with the alpha twins, who have taken Jennifer hostage. Kali challenges Derek to a fight one on one. They fight, and Derek holds his own while waiting for everyone else to arrive and turn the power back on. When they do, Boyd gets thrown into the fight, and Kali and Derek receive shocks as well. The alpha twins grab Derek's arms and hold his claws out so Kali can impale Boyd on them. Because Derek is an alpha, the wounds are fatal, and he absorbs Boyd's power as he dies. Derek is horrified and his hands shake as he stares at Boyd's body. Stiles puts a hand on his shoulder to comfort him.
Young Derek runs through the woods to escape the Argents. They aren't after him, but they're willing to take him since he's there. He and Peter hide under the nemeton to get away. At school, Derek and his friends mess around with a basketball outside the music room, much to the annoyance of Paige. Derek plays it too cool with Paige at first, but he impresses her with his wit and they start dating. They often went to the abandoned distillery to make out. She's concerned that he only likes her because she's a challenge, but before they can resolve that, Derek smells blood. They leave before packs of Werewolf come in.
Derek's affections are genuine, as shown by him listening to Paige play the cello while he's in class and his insistence on her confirming that she loves him. He and Paige don't eat lunch together because she doesn't like his friends. Peter convinces him that he needs to have Paige turned if he's going to spend his life with her. Peter's plan is to have an alpha other than Talia turn Paige. Derek goes along with it up until he hears Paige screaming in pain the night Ennis gives her the Bite, but he can no longer save her. She rejects the Bite, and Derek brings her to the nemeton. He cries and tries to comfort her. She reveals that she knew he was a Werewolf and didn't care. Derek mercy kills her when she can't take the pain anymore. The sacrifice gives power to the nemeton. This is how Derek got his blue eyes. It's revealed that in the present, he's gone to the abandoned distillery and is looking at the revenge spiral that Ennis carved there years ago.
Derek shows up at the school during Jennifer's lunch break just to see her and let her know that he's back after disappearing for a few days. They kiss. Derek asks her to come back to the loft with him, but she can't because she's organizing a recital that evening in honor of the recent dead.
Cora fights with Aiden and gets hit with a weight. Somehow, this does a lot of damage to her, and she ends up in the hospital. Derek arrives to watch over her and promises not to leave her side. While he's there, he hears Lydia's first banshee scream.
Jennifer finds Derek at his loft after she's taken Sheriff Stilinski as a sacrifice. She hugs and kisses him, but he doesn't respond like she expects. She realizes that Stiles and Scott were already there and had accused her of being the darach. She acts like that's crazy, but Derek looks at Stiles, crying, and asks her if it's true. She realizes that he believes Stiles more than he believes her. When Scott uses mistletoe to reveal her true self, Derek grabs her by the throat and threatens to kill her. Stiles and Scott beg him not to because they need her to tell them where the Sheriff is. She also claims she can save Cora. They go to the hospital, and Derek tries to talk to Jennifer as little as possible.
In the hospital, they learn that the alpha pack is already there. While Derek and Scott fight the twins, Jennifer escapes. They find Cora and run from the twins. Derek notices that Stiles isn't following and tries to stop him as Stiles hits the twins with his bat, but isn't fast enough. They get away and enter an exam room. When Stiles starts to yell, Derek lets him yell at him in frustration, knowing what Stiles is going through from having lost his own family. Jennifer shows up trying to make a deal, and Derek throws himself at her while pushing a table in front of Stiles to prevent him from doing the same when she mentions Stiles' dad, although Scott stops him. Derek and Peter learn that Scott is going to be a True Alpha.
While figuring out a way to distract the twins, Stiles picks up the paddles to a defibrillator and asks if they could be useful. Derek, the only one to pay attention to Stiles, asks if he knows how to use them and tells him to put them down when he says he doesn't know. Scott finds a needle of epinephrine, which Derek identifies and notes will only make the twins stronger. Peter uses the epinephrine on himself and he and Scott distract the twins so that Derek, Stiles, and Jennifer can get Cora to the ambulance. Kali is there, though, so Derek entrusts Stiles with Cora before he and Jennifer run. They get into an elevator and get stuck. Jennifer tries to explain herself, but Derek doesn't want to hear it. She hopes that the thing he isn't most upset about is that her real face is so ugly. She explains the connection between her second chance at life and Paige's death. Her plans is to use the lunar eclipse to kill Deucalion and [the alpha pack]], because they will be powerless but she won't be.
She knocks Derek out and escapes.
Derek comes to with Stiles about to punch him awake and immediately asks about Cora. Stiles insists that they have to get Derek out of there before the cops arrive. He meets the Argents and Isaac at a prearranged rally point and takes Cora. He and Isaac head back to the loft. Upset, Isaac yells at him for making them into Werewolf and putting them in danger and then just sitting there watching Cora instead of helping. Derek doesn't know what else to do. He spends all night siphoning off Cora's pain. Peter convinces him to use his alpha spark to heal Cora, trading his power for her life, although it means he won't have a chance against Kali.
Derek doesn't care. That night, he sacrifices his alpha power to save Cora.
Healing Cora takes most of Derek's strength, and it takes him nearly a day to recover. Ethan shows up to warn him that Kali and Aiden are coming for him before the lunar eclipse, and Peter convinces him to run. He and Cora start driving out of town. They turn around, however, when they hear Lydia scream. Derek finds Jennifer and Lydia at the loft. Jennifer tries to make a deal with him. If he agrees to be her guardian, she won't have to sacrifice the parents. She needs him because she can't take on Deucalion and Scott by herself. Derek agrees to help to save more people from being sacrificed. He and Jennifer meet Scott and Deucalion at the distillery.
Deucalion is more than Jennifer and Derek can take on. They lose handily until the lunar eclipse hits. Then Jennifer switches to Darach form. She's about to kill Deucalion but Derek stops her. He tricks her into using some of her power to heal Deucalion's sight, which leaves her weak. She can't kill Deucalion and Derek doesn't want to. He tells her to let the parents go. Instead, she starts to hit him. She slams him into a barrel and keeps hitting him until the lunar eclipse time runs out. He throws her, and she surrounds herself with a mountain ash circle. Derek watches as Scott pushes his way into the circle and then Deucalion slashes Jennifer's throat.
Scott and Derek let Deucalion live but order him to leave and never come back. Derek and Cora leave town as well, to bring Cora back to South America where she had been staying.
After leaving Beacon Hills, Derek and Peter get captured by hispanic hunters. They are chained to a metal fence and electrocuted. Derek rightfully blames Peter for their predicament.
Derek and Peter are tortured by the hunters, who demand to know where la loba is. Derek assumes they mean Cora, because la loba simply means female wolf. He refuses to give them any information and speaks to Araya Calavera in Spanish. Araya Calavera cuts off Peter's finger and leaves them to think about their fate. While she's gone, Braeden shows up to rescue them at Deucalion's behest. Derek insists that they get what they came for from the hunters' compound.
Derek and Peter return to the [[Derek's loft|loft], where Derek sews Peter's finger back on. He pointedly doesn't give him anesthetic. They open the box, which contains Talia's claws. Derek arranges the claws in the finger holes in the urn and has Peter jam his own fingers onto them. Peter then does a claw mind meld with Derek so Derek can talk to his mother. He has a vision of the loft with the nemeton in it, and his mother hops up onto the nemeton in her wolf form.
Derek comes out of the vision panting but won't tell Peter what he saw. Peter freaks out a little at him, thinking Talia must have said something about him.
Halloween night, Derek heads out of the loft to go shopping. No one else knows that he's back in Beacon Hills. He returns home at night and gives candy to some trick-or-treaters. He wolf's out at them just to scare them and is quite pleased with himself. Before he gets a chance to head up to the loft, Oni appear and knock him out. He wakes up a few hours later and howls, alerting Scott that he's back. Derek then discovers that his home has been turned into a party and he orders everyone out, throwing the DJ's table over. The Oni appear again, and they all fight, but the Oni vanish when the sun rises.
After the attack by the Oni, Derek follows Scott around town. He reveals himself when Scott gets home and the Oni try to attack. Scott, Melissa, Kira, Agent McCall, and the twins are all in the house. They throw the Oni out, and Melissa seals the house with mountain ash. The twins are curious what Kira is, since she can't cross the mountain ash barrier either. Derek calls them idiots and explains that Kira's a kitsune, though too young to be able to control her aura. He questions the twins' loyalty and willingness to die for Scott, implying that he is prepared to make such a sacrifice. The Oni start beating against the barrier, and as they are about to break through, Allison calls Scott to advise him to let the Oni perform their check. He does, while the others watch.
Derek gets a call from Scott telling him that Stiles has gone missing. It will be below freezing that night, so they have to find him. The sheriff's department finds Stiles's Jeep at the hospital, and Derek is first on the scene. He sweeps through the entire hospital following Stiles' scent and ends up on the roof. He explains to Scott how to read emotions from people's scents and asks him what he feels from Stiles's scent. He feels stress and anxiety. Derek confirms that Stiles was struggling with himself.
After everyone leaves to go to Eichen House looking for Stiles, Derek goes to jump start Stiles's Jeep. Aiden asks him what he thinks is going on. Derek scoffs at the idea that Stiles is the nogitsune, but as he's jumping the car, he makes a connection with the power outage and the nogitsune. The next day he asks Kira to show him what happened in the power station. He finds Stiles's bat magnetized and knows he was struck by a powerful shock. He asks Kira to explain to him about foxfire.
Later, Derek joins Scott in the hospital to wait for Stiles' MRI results. He tells him that Scott has to be the protector of Beacon Hills now, although Derek will help him. They realize that Stiles was trying to protect them and that's why he was on the roof. They return there and notice a cut power cable. When the nogitsune takes over Stiles, the power cable breaks free.
Derek and Scott hurry down from the roof to the parking lot, where people are getting killed by the power line. Isaac steps into some water and gets electrocuted before Kira can absorb the power from the line. Derek rushes to his aid and yells to Scott that Isaac isn't breathing. Derek insists that Scott tell the Sheriff what's going on. Stiles disappears, and Derek spends the next two days searching Beacon Hills for him.
Derek breaks into Chris Argent's apartment and leaves a sonic emitter jammed into his desk. When Chris gets home, they have a confrontation. Derek thought the emitter was a warning from Chris, but it wasn't. They talk about what Chris will do to Stiles when he finds him, and Derek doesn't seem pleased with the response. They discover that the case of money Katashi was going to pay for Chris's pistol is in Chris's closet, and then get arrested for Katashi's murder. Derek and Chris are taken down to the sheriff station and handcuffed to a bench. Chris asks for Derek to trust him while they try to figure out while they're being framed.
It turns out that there's a bomb in the sheriff station. While everyone starts to evacuate, they uncuff Derek and Chris, but there isn't time to get away. Derek throws himself over Chris to shield him from the blast. He is impaled with broken glass across his back, and Chris is stunned that Derek saved him.
Derek and Chris are locked up in adjoining cells in the sheriff station. Derek listens to the deputies talking out front and confirms that all the evidence from Katashi's murder is being moved. They discuss Stiles' situation and whether he's really in control of himself. Derek wants to know whether Chris will kill Stiles. Chris tells him about hunting a berserker, where he had to kill a teenager who was too far gone. Derek almost tearfully asks if Chris would feel remorse if he killed Stiles. Chris responds that he would, but not if he killed a nogitsune.
The charges against Chris and Derek are dropped, and they go to retrieve their things. Deputy Jordan Parrish doesn't want to give Chris his taser back, but Chris claims it's only for hunting. Derek gives him a deadpan look. The Sheriff then asks them both to come into his office. He shows them the brain scan of Stiles and explains that it's a fake. Stiles doesn't have his mother's disease, but thinking his does could break Stiles' resistance. He asks for their help in trapping the nogitsune. They go to the Argents' apartment and gather non-lethal weapons. The Sheriff gives them a chance to back out, but Derek says he isn't running from a fox. Derek points out that their plan now is the same as it was before, returning to the same places. The problem is they don't have a better plan. Derek spots Chris grabbing his gun.
They end up in Stiles's room, where the nogitsune has left them a clue in the form of the chessboard. Derek wonders why he's the king. This and why he is flanked by the twins' pawn pieces is revealed in 3x24 - The Divine Move. The clue leads them back to Derek's loft, where the nogitsune is waiting.
When the nogitsune refuses to come quietly, Allison, Chris, and Derek attack. Chris pulls his gun, and everyone starts shouting. Derek looks alarmed that Chris might actually shoot him. They delay long enough that the Oni appear, which was the nogitsune's plan. Everyone surrounds the nogitsune to protect him from the Oni, and they start fighting. Derek gets cut on the back of his shoulder. After the nogitsune vanishes, he gets out a chess set and starts setting up the board as he saw it in Stiles's room. Peter makes fun of him and points out that chess isn't a Japanese fox's game. Derek goes back to considering what Stiles' message could be and is infected with one of the nogitsune's flies, which alters his personality.
He goes to Chris's apartment with Talia's claws and shows them to him. He's very focused on how much the Argents have cost him, and Chris knows immediately that something is wrong. Derek is too quick for him, though, and ties him to a chair. He covers Chris in lighter fluid and threatens to set him on fire, but only when Allison is there to watch. Derek struggles with himself over what he's about to do, and his struggle gives Chris a chance to break free. Chris ends up with a gun to Derek's chin and begs him not to make him pull the trigger.
As Derek leaves, he asks Chris why he didn't' just kill him. Chris explains that they aren't enemies anymore. Derek thinks they should be out hunting the nogitsune, but Chris thinks they won't have to anymore because it will come for them.
Later, Derek finds Ethan and Aiden in the woods, shot with wolfsbane bullets. He helps them to the safety of a coyote den and then goes to get Chris to help transport them back to the loft. Derek pulls Chris aside and shows him shotgun shells he found in the woods. Chris recognize them but doesn't get a chance to explain before he gets a call from Allison and has to leave.
Derek finishes patching up the twins and, having made sense of Stiles' chessboard message, manipulates them into fighting along side him to save Stiles with the lure of earning their way into Scott's pack. While what he says about Scott is part of the lure, Derek doesn't seem to realize that what he says about Scott is much more true of himself - likely due to his low opinion of himself after everything he's gone through. Not thinking of himself as a hero is part of why he is one of the biggest heroes in the series. Instead of trying to keep up the image of being a hero, he does the right things and takes responsibility for stuff because it is the right thing to do and other people often won't step up.
Scott calls asking for the triskele urn that houses Talia's claws as they can trap the nogitsune inside it. Derek and the twins go to the high school where Scott, Stiles, and Lydia are planning the final showdown. The nogitsune is there waiting for them with some Oni. Derek and the twins fight, but they have no chance of winning until Chris and Isaac show up with silver arrows. Aiden retrieves the last arrow and stabs an Oni with it just as the Oni stabs him. Derek tells him that he'll tell Lydia that Aiden died as one of the good guys.
Some time later, Derek is in his loft when he's attacked by Severo Calavera and some Hispanic hunters. They are in turn attacked by someone else, who turns out to be Kate Argent. She shoots Derek, causing him to retreat into his mind's safe space as a defense mechanism where he's talking to Stiles, explaining what's happening. He asks how to tell if he's dreaming and Stiles tells him to count his fingers. Derek grabs Stiles' wrist and counts his. When he realizes that he's in a dream, he comes back to the reality that Kate is alive and just shot him.