The exact time that the Nogitsune was released from his prison within the Nemeton is unknown, but it can be assumed that it was at some point during or after the surrogate sacrifice ritual performed by Scott McCall, Allison Argent, and Stiles Stilinski in Alpha Pact/Lunar Ellipse, possibly assisted by the earthquake Jennifer Blake terrakinetically created in hopes of killing Noah Stilinski, Melissa McCall, and Chris Argent. A short time later, he possessed Stiles, but the Nogitsune, having been locked away for nearly seventy years, was presumably too weak to do much but observe Stiles' life and interpersonal interactions, gaining information about his host and his relationships while also trying to build up more power through feeding on the then-small examples of chaos, strife, and pain.
Sometime between his possession of Stiles and Galvanize, the Nogitsune managed to release some of his flies and used them to make William Barrow, a well-known mass murderer, his thrall. Under the Nogitsune's influence, Barrow captured the Thunder Kitsune Kira Yukimura, who was then unaware of her supernatural identity, and attempted to electrocute her so that her body would instinctively release foxfire as a defense mechanism. This foxfire was released just as Stiles, unknowingly acting as host for the Nogitsune, was walking into the electric substation with an aluminum baseball bat, leading him to be electrocuted enough that it jump-started the Nogitsune's power, giving him more control over Stiles' actions, the exact outcome the Nogitsune was hoping for when he began controlling Barrow.
In Illuminated, the effects of the Nogitsune started to influence Stiles' behavior more and more, starting with confronting Rafael McCall and revealing that he had learned the real reason as to why Rafael left the McCall Family at a young age. Stiles also found a mysterious key on his key-ring that he couldn't initially identify; after figuring out that it was covered in chemicals, Stiles realized that it led to the chemistry closet at Beacon Hills High School and that the code left on the chalkboard that instructed Barrow to go after Kira was in his own handwriting.
In Silverfinger, Stiles, who was suffering from insomnia and other exhausting side effects from being possessed by the Nogitsune, informed Scott that he believed he was responsible for somehow sending Barrow after Kira, though Scott had difficulty believing Stiles could do such a thing. He suggested Stiles go home and get some sleep, but Stiles instead went to Beacon Hills Memorial Hospital, where he confessed the symptoms he was experiencing to Melissa McCall, which included insomnia, irritability, inability to focus, sleepwalking, having vivid dreams during the day, and difficulty telling the difference between dreams and reality.
Melissa initially assumed his symptoms were a result of sleep deprivation and gave him a sedative to help him get a good night's rest, not knowing that by doing so, she had weakened Stiles' defenses and allowed the Nogitsune to gain even more control. When Stiles woke up a few hours later, he walked through the halls to find Melissa and was eventually confronted by three Oni demons, which, unbeknownst to anyone else, had been summoned to Beacon Hills by Noshiko Yukimura. However, when the Oni attempted to do their test to determine if he was possessed by the Nogitsune, the Nogitsune took over Stiles' body and killed all three of the Oni by plunging his fist into their chests and removing the firefly that animated them. Afterward, when Scott found him, Stiles/the Nogitsune played dumb and insisted that he was fine before asking him what he had learned that day, leaving Scott none the wiser about what he had done.
In Riddled, the effects of the Nogitsune's possession continued to affect Stiles as a result of the fact that they were constantly grappling each other for control over his body. Stiles eventually had such a vivid dream that he sleep-drove to the hospital, where he tampered with the electrical cords to the generator on the roof (while under the Nogitsune's control) before walking all the way to the Beacon Hills Preserve, where he ended up in Malia Tate's former coyote den; it has been implied that, on some unconscious level, Stiles knew what was happening to him and went into the woods on the coldest night of the year in hopes that he would die of hypothermia and prevent his loved ones from being hurt by the dark spirit inside him.
However, in Stiles' dream, he was in the basement of Eichen House (though he was unaware of it at the time), and the Nogitsune, in Corporal Rhys' form, had a conversation with him through his dreams. The Nogitsune was desperately trying to get Stiles to wake up so they could save themselves, since Stiles was beginning to suffer from hypothermia due to being in the woods in only his pajamas. To keep him conscious, the Nogitsune asked Stiles to solve a series of riddles, the last of which being "Everyone has it, but no one can lose it. What is it?" However, though Stiles could answer all of the previous riddles, it was the final one that he was unable to solve, and before he could figure it out, Melissa and Rafael McCall found him in the coyote den and woke him up.
Stiles was then brought back to the hospital, where Melissa confessed to Noah Stilinski that Stiles had the same symptoms as his mother, who was eventually diagnosed with frontotemporal dementia. This led Stilinski to immediately schedule an MRI for Stiles out, as he was concerned that Stiles had inherited the disease that killed his mother. During the MRI, the Nogitsune used his powers to trick Melissa, Stilinski, and Dr. Vandenburg into thinking that Stiles did indeed have FTD, while at the same time trying to convince Stiles to let him take control by threatening Stiles' loved ones. Eventually, Stiles figured out the answer to the Nogitsune's earlier riddle, "a shadow," just as the Nogitsune, in his bandaged Rhys form, unraveled the gauze from his face to reveal that Stiles was underneath, indicating that the Nogitsune was Stiles' shadow.
Stiles finally acquiesced and gave up control over his body in favor of saving his family and friends, and the Nogitsune (who will be referred to as Void Stiles while he is in full control of Stiles' body) prepared to walk out of the hospital inside of Stiles to continue his plans. However, he was confronted by Noshiko and two of her Oni in the elevator, where she asked him if he remembered her. The Nogitsune acknowledged that he did remember her before insisting that he "wasn't afraid of her little fireflies." Noshiko then told him that she wouldn't be deterred by the fact that he chose an innocent teenage boy to be his host, and that if the Oni couldn't defeat him, she knew someone else who did, implying that it would be her daughter Kira to finish him off.
At some point between Riddled and Letharia Vulpina, Void Stiles killed Katashi, an elderly member of the Yakuza who had given the Argents information regarding Kitsune and Nogitsune, before then framing Chris Argent and Derek Hale for the murder by planting evidence in the Argent Apartment, hoping that their arrest would prevent them from interfering with his plans.
In Letharia Vulpina, the electrical wire that the Void Stiles tampered with ended up electrocuting several people, all of whom died except for Isaac Lahey, who survived due to his Werewolf healing but who still needed to be put in intensive care as a result of his burns. After two days of being missing, the Nogitsune returned to Beacon Hills High School and pretended that Stiles was in control before orchestrated a series of mishaps to gain more power-- he set up a fake bomb on a school bus, a real bomb in the Sheriff's station, and a trap that caused Coach Finstock to be shot in the stomach with an arrow.
After feeding on all the chaos the events caused, Void Stiles also manipulated Scott into taking pain from three different people-- Isaac, Coach, and a dying deputy-- so that the Nogitsune could absorb and feed on all of the pain and become even more powerful as well. While Void Stiles was torturing Scott with a ninjato, Alan Deaton arrived and injected Stiles/the Nogitsune in the neck with a rare form of lichen known as letharia vulpina, which temporarily weakened the Nogitsune and gave Stiles control of his body once again.
In Echo House, Stiles decided to take advantage of the Nogitsune being weakened by admitting himself into Eichen House, hoping that by doing so, he would be protecting his family and his pack. However, though the Nogitsune was weakened, Stiles was still suffering from hallucinations of the bandaged version of him. Additionally, with the Nogitsune weakened, Stiles developed a Lichtenburg figure on his back from when he was electrocuted with Kira's foxfire, since he didn't have the Nogitsune's healing ability working at peak performance. When Marin Morrell, the therapist at Eichen, noticed the Lichtenburg figure, she took Stiles aside and gave him a bottle of amphetamines to stay awake, as sleep would make him vulnerable and allow the weakened Nogitsune to regain control faster. She then informed him that if the McCall Pack hadn't come up with a solution by the time his marks faded, she would come find him and give him an injection of pancuronium bromide, a drug used in lethal injection to induce respiratory arrest that she believed would neutralize the Nogitsune once again by killing Stiles.
However, despite Stiles' best efforts to stay awake, he was caught with the amphetamines by the head orderly, Brunski, who injected him with Haldol and locked him in the "quiet room" to sleep it off. Fortunately for him, Malia Tate found him and rescued him, taking him down to the basement in hopes of finding answers about the Nogitsune. While down there, he and Malia found Corporal Rhys' bandaged body (the same form that the Nogitsune takes while in Stiles' mind) hidden in a wall that had been marked with the jiko kanji to indicate that he died as himself. Along with his body, they found Noshiko's broken magic katana and a photograph of Noshiko and Rhys, which led Stiles to realize that the Nogitsune and Noshiko are connected. However, before he could do anything more, a fellow Eichen House patient, Oliver, revealed that he had become one of the Nogitsune's fly-thralls, and used a taser and Haldol to knock both Stiles and Malia out. The Nogitsune then threatened to have Oliver kill Malia by drilling a hole in her head (a procedure known as trephination) if Stiles didn't once again let him have control. Stiles, not wanting her to get hurt, eventually gave the Nogitsune what he wanted, and Void Stiles the used the drill to knock Oliver out before he escaped Eichen House.
In The Fox and the Wolf, after Void Stiles left Eichen, he went to the high school, where he found Ken Yukimura preparing for Monday's class in his classroom. The Nogitsune physically threatened him and admitted that he had no idea how Noshiko was able to create physical representations of her tails by making them into black ceramic daggers before demanding to know the location of the sole remaining dagger, which she calls "kaiken." When Ken played dumb and refused to answer, Void Stiles summoned one of his flies and had it forcefully fly down Ken's throat, believing that making him a fly-thrall would get him answers. Unfortunately for Void Stiles, Ken resisted the effects of the fly and was eventually cured with reishi mushrooms by Noshiko, Kira, and Scott before he could learn the location of the kaiken, which was in Noshiko's jacket pocket.
Scott and Kira then showed Noshiko the photo Stiles and Malia found on Rhys' body before demanding that she tell them the story of the Nogitsune. (see "Early Life" above). Meanwhile, Void Stiles went to the Stilinski House and set up Stiles chessboard with all of the pieces the real him had used to create the board game that helped introduce Sheriff Stilinski to the supernatural. ("The Girl Who Knew Too Much") Seeing that the king was labeled "Derek Hale," Sheriff, Derek, Chris Argent, and Allison Argent went to Derek's loft, armed with all of the non-lethal weaponry the Argents possessed, to try to take Void Stiles alive until they could figure out how to exorcise him. When Sheriff walked in first, Void Stiles pretended to be the real Stiles when he greeted him.
In De-Void, Sheriff attempted to reason with Void Stiles, eventually talking him into allowing himself to be handcuffed so they could take him into the Sheriff's station, which he argued would both protect the innocent civilians from Void Stiles and protect Stiles himself from those who would try to do him harm as well, such as the Oni. However, when Void Stiles broke through the handcuffs with one hard tug, they realized that they were not talking to Stiles and fell to their backup plan. Chris, Allison, and Derek then flooded into the loft after Sheriff to confront Void Stiles with him; however, Void Stiles easily caught the taser bolts shot at him by Allison due to his enhanced reflexes and electrical immunity, the latter of which allowed the electricity to pass harmlessly through him. Realizing Allison was no match for him, Derek wolfed-out, roaring at Void Stiles before lunging at him, but Void Stiles' supernatural strength was superior to that of the Beta werewolf and he threw Derek across the room.
When Chris reflexively pulled out his gun and aimed it at Void Stiles, he and Sheriff argued heatedly about whether or not they should shoot him while Void Stiles eagerly egged Chris on. After a few long moments, Allison realized with horror that the Nogitsune was feeding off of their strife and stopped them, leading Void Stiles to admit that they ultimately weren't going to be there to kill him-- they were now there to protect him. As Void Stiles predicted, the Oni demons appeared in the loft to attack him, forcing Sheriff, Chris, Derek, and Allison to reluctantly defend him in order to ensure Stiles' survival. At some point in the fight, Derek was injured by the Oni's ninjato, and Void Stiles mysteriously vanished, followed shortly afterward by the Oni.
Void Stiles then went back to Eichen House, where he found Noshiko in the basement, kneeling in front of the wall where she buried Rhys. He asked her why she carved the jiko kanji (which means "self") into the wall where his body was interred, and Noshiko replied that it was to signify that he died as himself and not as a monster like the Nogitsune. When Void Stiles asked her what happened to the woman who called out for chaos, strife, and pain in order to get revenge on those who covered up the riot at Camp Oak Creek in 1943, Noshiko insisted that she didn't want that anymore. Unfortunately for her, Void Stiles remarked that he did before stealing Noshiko's kaiken and using it to stab himself in the stomach, essentially disemboweling himself with the ceramic dagger.
From within the slice wound in his abdomen came a swarm of Nogitsune flies, which then escaped from his body and scattered across the town to create more thralls. One fly possessed Isaac Lahey by crawling through his IV catheter while in the ICU at the hospital; possessed Derek Hale by crawling into the gash on his back that was made by the Oni's sword; possessed Ethan by crawling up his nose while he was washing his face after lacrosse practice; and possessed Aiden by crawling into his ear when he found Void Stiles' unconscious body in a parking lot. All four men then became Void Stiles' thralls, and the Nogitsune flies removed their inhibitions and increased their preexisting anger so that they would attack the objects of their anger and create diversions while Void Stiles, continued to cause more chaos, strife, and pain on which to feed and become more powerful.
Lydia Martin and Aiden were driving together when Lydia suddenly went into a Banshee fugue state and drove to an empty parking lot where Void Stiles had fallen unconscious. They then brought him back to the McCall House, calling Melissa McCall and Alan Deaton to help them deal with him. It was there that they determined that Stiles had gained the Nogitsune's power of accelerated healing, and Deaton gave Void Stiles a dose of Kanima venom to paralyze him while they came up with a better plan on how to best help Stiles. After debating the merits and risks of Scott giving Stiles the Bite in hopes that the Nogitsune would be expelled upon his transformation into a werewolf, they eventually turned to Peter Hale for help; after Peter declared that Stiles was much too weak to survive the Bite, he instead suggested that he teach Scott to use the Alpha mind manipulation ritual. Scott then put his claws into the back of the neck of both Stiles and Lydia, allowing Lydia to accompany him inside Stiles' mind to try to take control back from the Nogitsune and give it back to its rightful owner.
Inside Stiles' mind, the Nogitsune attempted to distract them by locking them in separate memories or visions, with Lydia believing she was back at the Winter Formal in Season 1's Formality the night that she was attacked and bitten by Peter, while Scott was led to believe that he and Allison were still together and making out in her closet during the events of Season 3A's Currents. However, both of them managed to break out of this vision, where they found that the Nogitsune had locked Stiles' consciousness in "the White Room;" on the opposite side of the enormous room from where Scott and Lydia were standing, Stiles and the Nogitsune (in the form of his previous vessel, Corporal Rhys') were sitting on the Nemeton's stump, where they were playing the Japanese strategy game Go. Despite the Nogitsune's best attempts to keep the two from getting through to Stiles, Scott Alpha-roared at his best friend, alerting him to their presence and allowing Stiles to take control of his body back from the Nogitsune.
In the real world, Scott and Lydia were shoved out of Stiles' mind, and when they came to, they all watched in shock and horror as Stiles began throwing up the bandages that covered the Nogitsune when he used Rhys as a vessel. Once Stiles was done, the bandages materialized into what appeared to be Rhys' form once again, only separate from Stiles, but when Peter and Scott tackled him and tore off the bandages, they found that the real Stiles, who was completely overwhelmed and terrified, was inside. It was then implied that the Nogitsune had used all of the power he had gained from feeding on the exceptional amount of chaos, strife, and pain he created to create a new, completely whole and unblemished body for Stiles, keeping Stiles' original body for himself. The Nogitsune then escaped, still wearing Stiles' visage, and captured Lydia in the process.
In Insatiable, the Nogitsune held Lydia hostage in the tunnels at Camp Oak Creek, and seemed amused by the fact that Lydia, as a Banshee and a harbinger of death, was hearing the loud voices of all of the dozens of people who had died there in 1943, both at the Nogitsune's hands and during the riot that caused Noshiko to summon him in the first place. The Nogitsune explained that all of the mythical trickster stories about the coyote, the fox, and the raven were all about food, because tricksters are always hungry. He then stated that, as a fox and a trickster, he was the same, but instead of eating food, he said, "I eat what you feel," indicating that he gained sustenance from chaos, strife, pain, and tragedy, among other negative emotions such as fear and rage.
When Lydia asked why he took her, the Nogitsune confessed that he needed her Banshee powers so that he would know when his own death was getting close. When the Oni arrived and surrounded him, he took out one of Noshiko's last kaikens, which was among the oldest, and which he stole in the previous episode. Just as the Oni aimed the tip of their ninjato swords at him and prepared to impale him, Stiles broke the kaiken in half, using the immense mystical power inside to steal control of the Oni from Noshiko. With the demons now under his command, he ordered them to fight against Noshiko, Kira, Isaac, and Allison, while Scott and Stiles searched for Lydia, eventually finding her locked in a room in the tunnels. The Nogitsune looked shocked when Allison became the first person (aside from himself) to kill an Oni, which she accomplished by shooting it in the chest with a silver arrowhead she had forged herself earlier that day. However, the Nogitsune got his revenge shortly afterward when another Oni stabbed her in the abdomen and killed her.
Allison's death caused the battle to end, as both the Nogitsune and the Oni vanished out of fear that the pack could find ways to kill the rest of them while the pack and Allison's father dealt with immediate aftermath of her loss.
The next day in The Divine Move, the rest of the McCall Pack and their parents and allies regrouped to come up with a new plan to take down the Nogitsune once and for all, eventually finding the four remaining silver arrowheads that Allison had made prior to the battle to kill the Oni and discovering that the Hale Family's Triskelion urn was made by Alan Deaton using wood harvested from the Nemeton, making it powerful enough to contain the Nogitsune once again in its fly form. While they were planning their final battle against the killer of their dear friend and loved one, the Nogitsune led the Oni to the Beacon County Sheriff's Department, Beacon Hills Memorial Hospital, and Beacon Hills Animal Clinic, where they sliced as many people as they could find with their mystical-poison-coated ninjatos that caused their wounds to excrete black smoke; Sheriff Stilinski, Jordan Parrish, Melissa McCall and Alan Deaton were among the dozens who were injured, and many of the others died before the poison's effects could be reversed.
After their plan was in place, the pack then split up, with Aiden, Derek, and Ethan fighting against the Nogitsune (still in Stiles' original body) and his Oni outside the high school while Scott, Stiles, Lydia, and Kira went inside to enact their plan. However, upon entering the front doors, the high school's interior turned into the garden in Japan where a young Chris Argent and a branch of the Yakuza (whose members included Katashi and the Kumicho named Ikeda) were attacked by Oni twenty-four years earlier ("Silverfinger"), revealing that the Nogitsune had used his considerable powers to create an elaborate illusion.
Scott and Kira fought against the Oni and the Nogitsune (in Rhys' form) after the Nogitsune claimed that the only way to prevent everyone who had been sliced with the Oni's blades from dying was if Stiles performed sepukku (a ritual self-disembowelment that was utilized by Japanese samurai) on himself and allowed Scott to perform the killing blow by decapitating him. However, they eventually realized that everything around them was an illusion and were able to break out of it. They then found themselves back in the real world in the high school, just as Derek and the twins, aided by Isaac, Chris, and Allison's silver arrowheads, killed the remaining Oni, though not before the last Oni killed Aiden first, making him the McCall Pack's second casualty in the war against the Nogitsune.
Inside the school, the Nogitsune was furious that he was outsmarted by the pack, insisting that they couldn't beat him at his own game because he was 1,000+ years old and couldn't be killed. However, Stiles and Lydia reminded him that they could change him, as they learned from the Shugendo scroll, and before the Nogitsune could react, he was bitten on the shoulder by Scott before being stabbed through the chest from behind by Kira and Noshiko's magic katana. This caused the Nogitsune's vessel (Stiles' original body) to crumble to dust, leaving only a single Nogitsune fly left behind, which Isaac quickly trapped in the Triskelion urn. Afterward, the urn was taken to France by Chris and Isaac, and is presumably in a safe place to prevent the Nogitsune from returning to cause more trouble in the future.