In the late 12th century, Merlin catches his apprentice Hisirdoux "Douxie" Casperan in the act of using magic to finish his chores. Douxie wants to be "a real wizard like [Merlin], with a staff and everything," but Merlin tells him it takes time to master the magic needed to have one. In present day Arcadia Oaks, Douxie and his familiar, Archie, are summoned by Merlin after centuries of waiting. Something dire is afoot, and Douxie is instructed to gather the heroes of Arcadia. However, Archie can only find Tobias Domzalski, Steve Palchuk and AAARRRGGHH!!! the troll and takes them to their secret lair hidden in a bookshop. There, they and Merlin are attacked by monstrous shadow mephits and a strange figure in green medieval armor before retreating on an airship that Merlin conjures from a snow globe.

The teens reunite with Claire Nuñez and Blinky in Camelot Castle – now a flying air fortress powered by the mysterious Heart of Avalon – where they learn that Jim Lake Jr. the Trollhunter was attacked with a onyx shard wielded by the mysterious Green Knight, who Merlin discovers is somehow connected to his fallen apprentice and archenemy, Morgana le Fay. The onyx shard that wounded Jim is slowly killing him, so Merlin encased him in green crystal to stall its progress. Suddenly, the Arcane Order – an evil organization of demigods brought by the Green Knight – attacks Camelot, killing Sir Galahad and forcing Merlin and his wizard companion Nari to open a rift in time. However, during the attack, Claire, Steve, Douxie and Jim all fall into the past and awaken in Camelot's forest, where they are confronted by Sir Lancelot and his men.

Upon their crash-landing in the Mid-12th Century, Jim breaks free from the crystal and finds himself alive, despite the onyx shard from the Green Knight's spell still wedged in his chest. However, because he is half-troll and gets petrified in daylight like one, the Knights capture him, Claire, Douxie and Steve and take them to King Arthur and his court, which includes his sister Morgana – which infuriates Claire because she had tried to possess Claire's body one year ago. However, Douxie and Morgana convince Arthur to spare Jim's life, even though he ends up trapped in a dungeon with other trolls, and Morgana adopts Claire as her new handmaiden (secretly interested in Claire's Dark magic that she used to save Jim), while Steve trains to be a knight under the command of Lancelot. Meanwhile, Douxie returns to his old living space and seeks Past Merlin's help in accessing the time map to return them home to Arcadia Oaks without further altering the timeline.

Having staged a dungeon break, Douxie and Claire work covertly to get Arthur and Morgana le Fay to reconcile, but with Past Merlin and Archie getting involved, Douxie is getting on his master's nerve. Meanwhile, Jim and the other trolls who were freed are now living in the Wild Woods, protected by a younger Gunmar and his son Bular. However, despite the group's efforts, Jim's new friend Callista gets hurt, Bular is captured by the knights, and Morgana, enraged by Arthur's stubbornness, turns against the rest of Camelot's people when they try to kill Jim and Claire in front of her. But, as they battle, Arthur cuts off Morgana's left hand with Excalibur and watches as she falls to her death off a cliff and disappears into the waters below.

In the end tag, Arthur and Claire grieve Morgana's demise and Jim (seemingly on the brink of death) crosses paths with a younger version of his troll mentor Blinkous Galadrigal/Blinky.

Merlin leads a ragtag group on a mission to collect and reconnect the broken pieces of Excalibur. Meanwhile, Claire's been having nightmares about Morgana and Jim as her dark magic seems to be getting stronger, and Jim tries to convince a young Blinkous Galadrigal that they're on the same side only for an evil AAARRRGGHH!!! to attack the troll sanctuary of Dwoza. Eventually, after teaching Claire to control her shadow magic without Morgana's staff, Douxie's group encounter Nimue, the Lady of the Lake, who reveals herself to be a vicious kraken. She reveals to the teens that Merlin trapped her in the cave long after she gave him Excalibur and she attacked them in the attempt to get her revenge. After breaking down the Cave wall with one of his spells, Douxie earns Nimue's trust and she agrees to repair Excalibur. In the show's end tag, Angor Rot discovers Morgana's body and brings her to the cave of the Arcane Order, who revive her and give her a new left hand to replace her old one.

Having been revived by the Arcane Order (consisting of a younger Nari, Skrael, and Bellroc), Morgana gains new powers and golden battle armor and dubs herself the Mother of Monsters, vowing to bring in an Age of Reckoning by fighting for all magics. Meanwhile, Douxie continues training Claire when she overhears Morgana plotting in the Shadow Realm and accidentally contacts her. Having barely escaped with their lives, Archie and Claire must form a counterattack for when Morgana returns to Camelot. Meanwhile, Jim and Callista try to defend Dwoza from Gunmar and his general AAARRRGGHH!!!, who are angry about Bular being held prisoner in Camelot. Jim's actions inspire both Blinkous and his brother Dictatious to lead a revolt to drive back Gunmar's presence in their village and Callista successfully captures AAARRRGGHH!!!. Jim suggests they rehabilitate AAARRRGGHH!!! and Vendel, the future leader of Trollmarket, puts the fallen general under the watchful care of Blinky.

Back in Camelot, Claire dons her armor and poses as a knight named Sir "Clairee", as she exposes a changeling sent by Morgana to free Bular and assassinate Arthur. Douxie and his group come to Arthur's rescue, despite a bombing of the castle walls allowing Bular to escape, and they capture the changeling spy. In the end tag, Morgana approaches Gunmar and proposes an alliance.

To defend what's left of Camelot, King Arthur seeks an alliance with the good trolls living in Dwoza, and Claire tries to reunite with her boyfriend. Meanwhile, AAARRRGGHH!!! and Blinky's friendship begins, Morgana enchants Gunmar's Decimaar Blade to control minds, and Douxie and Merlin finish building the Trollhunter's amulet, with Merlin promoting Douxie to the rank of Master Wizard with his own staff. Then, the amulet chooses Callista to be its first wearer. The trolls reject Callista at first and they refuse to join in the battle. However, the battle for Killahead bridge begins regardless. In the end tag scene, Callista reads a rock with troll writing, translated "Deya." Accepting her new role, she renames herself Deya the Deliverer and sets the stage for the original Trollhunters timeline.

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Despite our heroes' best efforts, Sir Lancelot and King Arthur are killed by Bular and Bellroc in the battle for Killahead Bridge after the Arcane Order decide to make themselves known and partake in the mass carnage. Just as all seems lost for the humans, Deya leads the trolls into battle to aid the humans. When Deya and Gunmar are at the bridge, she places the amulet on the side of the large construct, which opens the portal into the Darklands causing Gunmar and the Gumm-Gumms to be sucked in. At the same time, Claire, Douxie and Merlin succeed in imprisoning Morgana, with Claire foreshadowing their next and last encounter in the future and sending her across the world to where she is imprisoned in the realm of Trollhunters.

After returning home to Arcadia in the 21st century, and destroying the high school with Camelot's crash-landing, the team reunites with present-day Merlin, Toby, Blinky and AAARRRGGHH, and learn how Nari defected from the Arcane Order and sought protective asylum. However, the Arcane Order attacks and the Green Knight pushes the onyx shard closer into Jim Lake's chest. Jim sacrifices himself by pushing the shard completely into his chest, turning into a full troll and allowing him to fight back before he weakens. However, Troll Jim becomes enslaved by the Green Knight, who is soon revealed to be a resurrected Arthur, now under the spell of Bellroc and Skrael. The Order then takes the Amulet of Daylight and destroys it in a ritual to resurrect Morgana and re-induct her into their ranks. In the end tag, Arthur, revealed to be the Green Knight, kills Merlin and the wizard leaves behind a mysterious book for Claire and Douxie to safeguard.

In a flashback, we learn how Merlin adopted Douxie and Archie by saving them from persecution in the streets of Camelot by Sir Galahad. In the present, Archie and Douxie, along with Claire and Steve, mourn Merlin's death. To stop the Arcane Order, Archie and Douxie visit Archie's father, a large dragon named Charlemagne the Devourer, aka 'Charlie', to help translate Merlin's Grimoire in order to determine the location of the Genesis Seals. While Krel, Steve, and Toby keep watch over Nari, Claire enters the shadow realm to find Jim's soul.

Meanwhile, Morgana realizes that her interests are no longer aligned with the Arcane Order, and she must try to repair her relationship with Arthur; she leaves for the shadow realm to find her brother's soul and free him from Bellroc and Skrael's influence. Morgana and Claire help each other in the shadow realm, but neither are successful in saving Arthur or Jim's souls; Jim is being torn apart, and Arthur brought Morgana back from the dead so that she could see him and the Order kill Merlin. Morgana is now on the side of the Trollhunters and wizards of Arcadia. At the end tag, the Order follows Morgana to Hex Tech, the Trollhunters' final hiding place.

Returning to Arcadia, Douxie tries to protect Nari from the Arcane Order and retrieves Krel Tarron from the wreckage of a fight at Hex Tech. The other heroes are bound by Bellroc & Skrael aboard the Arcane Order's flying castle. Douxie delays the Order using a time loop built from the remains of the Heart of Avalon so he can rescue the others from the ship. He frees Nari from the Order after Morgana sends herself and Arthur flying out a window.

Morgana and Arthur battle each other on the ground, while Claire, Toby, Blinky, and AAARRRGGHH!!! desperately try to save Jim's soul. As Morgana sacrifices herself to squish Arthur, Jim turns into stone and dies. As Claire hugs Jim's stone form and cries, a tear falls off her cheek, landing on stone Jim and causing him to crumble. From the rubble rises Jim in his original human form, but he no longer has the Amulet of Daylight or the powers of the Trollhunter. When Arthur died, Excalibur is stuck in a stone. Meanwhile, Douxie is gravely injured in his battle with the Arcane Order, who escaped the time loop. The spirits of Douxie, Morgana and Merlin have a final conversation in Merlin's old library/workshop before Morgana and Merlin walk through a door into a bright light and Douxie's soul returns to his body. Douxie vows to spend the rest of his life protecting Nari from the Arcane Order to prevent the breaking of the Genesis Seals. Jim and Toby both try to remove the sword from the stone, but to no avail. Douxie, Archie and Nari leave on Merlin's airship while Jim, Claire, Toby, Steve, Blinky, AAARRRGGHH!!! and Krel remain behind as the champions tasked with protecting Arcadia from future threats, but Douxie promises to return in the near future. The series ends a short while later, with Nari and Douxie walking on a street in a city while Bellroc watches them from atop a building, plotting their revenge.