Dragon Knight Davion from the Dragon's Hold and his squire Bram are enlisted by the village of Barrowhaven, to help slay a lone earth wyrmling. After defeating the wyrmling, Davion and Captain Fruhling, the leader of the local soldiers, discover an underground dragon nest where an Eldwyrm is slumbering deep within the tunnel system. Knowing the danger of confronting an Eldwyrm, Davion chooses to let it sleep, and returns to the village, much to Captain Fruhling's disapproval. While celebrating in the tavern, Davion encounters Mirana and her handmaiden Marci, who are there to meet with a hooded elven named Gwanwyn, for information regarding their lost Lotuses. A skirmish with a drunkard leads to Gwanwyn getting exposed as an elf. As elves are hated amongst the humans, Davion is forced to toss him out to save him from being beaten up. Gwanwyn then instructs Mirana to seek for Nikdo in Haupstadt. Meanwhile, Terrorblade, a demon imprisoned among the fractured walls of Foulfell, possesses the body of Fruhling and puppeteers him to return to the Eldewyrm.

In a flashback, it is revealed that Fymryn stole the lotuses from the pools of Selemene's temple in Nightsilver Wood. She uses her disguise ability, teleportation and duplication ability to escape the pursuit from Mirana and Marci, who serves the Dark Moon Goddess Selemene. Blaming herself for failing to stop the thief, Mirana and Marci take it upon themselves to leave Nightsilver Wood to retrieve the lotuses from the thief.

Fymryn brings the lotuses back to the Coedwei forest enclave, one of the enclaves occupied by the Coriel'Tauvi, an elf race who worships the goddess Mene after being outcast by Selemene from Nightsilver Wood for refusing to worship her. Fymryn and the Coriel'Tauvi believes that their goddess Mene has been trapped in the shadow by Selemene, and Fymryn intends to fulfill a prophecy of bringing Mene back so that they can overthrow Selemene and return to living in Nightsilver Wood. To do so, she embarks on a journey with fellow Coedwigs inhabitants Adara, Dyfed and Idwal to the Broken's Peak to find the Invoker, believing based on the story that he could use the Lotus to bring back Mene. Upon reaching the tower, the Invoker is shocked that she can locate his hidden tower. He takes the Lotus from her, gives her a coin with a face of Mene, and sends them back out to the woods instead of helping them. Having failed the mission, the team decided to spend a night in the forest. Luna, worshipper of Selemene, arrives and demands them to return the Lotus, while murdering all of them except Fymryn, who was saved by the Invoker.

Mirana and Davion reach a Dragon Knight fortress in the mountains, and they are soon joined by legendary Dragon Knight, Kaden. Kaden reveals to them that he is on a revenge quest against Slyrak, after Slyrak murdered 29 of his fellow Dragon Knights almost 20 years ago in the city of Leathsham. Since the incident, Kaden started slaughtering dragons and forged armor from their corpses to prepare himself for the fight against Slyrak. The revelation leaves Davion in a conflicted position. Despite keeping quiet, Kaden quickly deduces that Slyrak is hiding inside Davion, as he injured Davion to draw Slyrak out. The ensuring battle between Slyrak and Kaden destroys the fortress, while Slyrak carries Marci, Mirana and Sagan to escape.

Following Davion's fight with Kaden, Slyrak goes on a rampage while Davion's consciousness is trapped in communion with the other Elder Dragons on the Thunder Plane. Davion encounters the other eldwurms (Aethrak, Lirrak, Byssrak, Indrak, Orrak and Vahdrak) and they exchange information, while a disoriented Slyrak attacks Marci, Sagan and Mirana. Davion and the Eldwurms deduce that a demon called Terrorblade is hunting them, and that Slyrak has permanently bonded himself to Davion. Sensing Slyrak is going to kill Mirana and the eldwurms not wanting Davion in the Thunder, they kill Davion to bring Slyrak back to the Thunder and Davion back to the real world.

Luna serves as Selemene's weapon in the battle to subdue the rebel enclaves of the Nightsilver Woods and force the inhabitants to declare their loyalty to the Dark Moon. Selemene bestows her power to Luna and the Dark Moon Order, allowing them to capture Drysi, the Elven Legion leader while killing everyone else in the Elven Legion effortlessly.

Mirana and Davion reach the Invoker's tower and seek his help. The Invoker reveals to Davion that the eight souls of the eldwyrms that the Terrorblade is collecting, serve as the eight pillars of creation that support all of the realms and the infinite realities, and that Terrorblade intends to use the souls to remake the world in his image. In order to help Slyrak soul who is hiding inside Davion, the Invoker imbues a spell to prevent Davion from turning into Slyrak or Slyrion, but the process will kill Davion eventually. The Invoker also rejects Mirana's opinion of Selemene, but nevertheless agrees to return the Lotus to her on the condition that she order her troops to withdraw from Coriel Tauvi's enclaves.

The Invoker seeks out Lirrak, and proceeds to steal her soul. While recuperating, he thinks back to the memories of his daughter Filomena. It was revealed that Selemene and the Invoker were once a couple, but separated after Filomena and the Invoker chose not to worship her. Their relationship strained further when Selemene refused to cure an ill Filomena, whom she had poisoned to lure the Invoker back to her, after Filomena insisted to refuse worshipping her, letting her daughter die.

Kaden, having survived the ordeal against Slyrak, continues his pursuit of Davion with Bram and fellow dragon knights.

While entering the Coedwei forest, Davion's team discovered and buried the Legion's corpses who were killed by Luna's Dark Moon Order, before venturing to the village within the forest. Reaching the village with the shrine, now occupied by Luna's Dark Moon Order and the surviving but imprisoned Coedwei elves, Fymryn left the group while Mirana handed the lotuses to Luna. Having accomplished the mission, Mirana prepares to return to her noble position while Davion contemplates parting ways. Fymryn attempts to rescue Drysi, who rejects her help because she now chooses to stop hiding and that Selemene's attacks has given them back their taste for blood.

Stripped of her divinity, Selemene warns the Invoker that he is making a mistake for making a deal with the demon. Invoker rejected her plea to return her power. Meanwhile, Mirana and Marci accompanied Luna and the surviving Orders members, who are starting to lose faith in Selemene for failing to assist them after returning the Lotuses.

Kaden and the team brought Davion back to see the Father, leader of the Dragon Knights, at the Dragon's Hold. While resting, Ritterfau, veteran Dragon Knight, bickered with Kaden over bringing a Dragon Knight back as Slyrak. Meanwhile, Father started experimenting on Davion. Fymryn tries to rescue Davion, who rejected her help after learning that she had previously secretly agreed to bring him back to the Invoker after returning the Lotuses. Later on, Fymryn discovered Father's experimental plan of transfusing his blood to let himself transform into a human/dragon hybrid and gain the power of a dragon.

Despite best efforts from Ritterfau and the Dragon Knights, the swarm successfully massacred the knights and destroyed the fortress, while Bram inherited Ritterfau's sword. In order to stop Terrorblade from manipulating Bram, Kaden and Davion and Fymryn to let him possess their body, Fymryn killed Father, body vessel to Terrorblade. Rylai and Auroth arriveed to save Bram, Davion, Kaden and Fymryn from the swarm and brought them back to her home.

Wanting to fulfill its purpose of creation by bringing chaos, Vahdrak betrayed and killed fellow Eldwyrm kins Orrak, Indrak, Byssrak, Aethrak, allowing the Invoker to collect their souls, including Vahdrak's.

Davion's group take shelter at Auroth's cavern, and discovered a mysterious ore in Auroth's possession, which transformed Auroth many years ago by giving her the ability to converse with humans and turn into human form, but removed her ability to communicate with other Eldwyrms. Davion used the ore to talk to Slyrak, who instructed him to seek the Eye of Worldwyrm at the Helio Imperium, so Slyrak can travel to Foulfell to kill Terrorblade.

Fymryn leaves the group to try and convince her people from starting a war, while Kaden departs to rebuild Dragon's Hold. Rylai instructs Davion to find her sister, Lina at the Helio Imperium so she can help Davion meet the emperor. Davion heads to the Helio Imperium with Bram and Auroth, who takes human form before entering the capital.

Mirana attempts to bargain for an army to reclaim Nightsilver Wood as a marriage term, but was rejected by war council member Legatus Tihomir, who funds the troops.

The Invoker relinquishes Lirrak's soul to Terrorblade but refuses to hand over the rest of the dragon souls, citing his refusal to aid Terrorblade's plan. Terroblade leaves after issuing a threat.

After learning more about Filomena, a remorseful Selemena, apologizes to the Invoker, who is troubled with Terrorblade's threat.

Auroth, Davion and Lina deduce that Mirana is neither dead or alive. Davion meets with Emperor Shabarra to seek the Eye, but is rejected. Davion transforms into Slyvion and kills Shabarra.

Luna and Nico track Virani down and discovers the person who hired her: Lina. Lina knocks out Luna and flees the scene, while Marci arrives to help Luna.

Marci, Sagan and the surviving Dark Moon Order soldiers, having escaped Vinari's kidnapping wagon thanks to Sagan, regroup with Luna. Lina confronts Slyvion, who feels a connection with Lina, declaring that Lina is a child of fire and therefore a part of him. Luna turns him back to Davion to stop his rampage against the Praetorian Guard. Davion pledges support to Lina to become a regent.

Following Shabarra's death, the morning sun shines onto Mirana, bringing her back to life.

Mirana returns to the Senate, surprising everyone including Davion, to declare her desire to take over the ruling from Emperor Shabarra. Her appeal attempt failed when the Senate chooses to elect Lina as the regent, with support from Tihomir.

Learning the truth, Mirana tasks Luna and the Orders to return to the Nightsilver Wood and wait for her, while she returns to the castle with Asar, Bram, and Auroth.

With the help of Lina, Davion finally accesses the Eye but, when nothing happens, he believes it's a forgery. Fymryn is tempted by Terrorblade, while the Invoker reveals to her she is the reincarnation of Mene and asks her to take the divine spark of Selemene, who's now powerless and held prisoner in his tower, to stop the Coriel'Tauvi, who has been driven mad by revenge.

Lina confesses to a desolate Davion that she hired the assassin who tried to kill Mirana, thinking that doing so would expose Shabarra as a fraud and that the Senate would make him abdicate. Feeling betrayed, Davion reconciles with Mirana.

Fymryn confronts Selemene and, instead of killing her, she brings her to visit Filomena's tomb: Selemene then regains her powers and flees the tower.

Davion and Mirana interrogate old Captain Asar about the night the Emperor was killed and they suspect that Kashurra has swapped the real Eye with the forgery. Meanwhile, Viceroy Kashurra kills Lina for trying to kill Mirana.

Having fled from the Invoker's castle, Selemene reaches Luna and the Dark Moon Order but they now reject her in favor of Mirana, leading Selemene to take her power back from them as she attacks Coriel'Tauvi. Viceroy Kashurra, now fully transformed into a Void Dragon, kills Auroth as she stall Kashurra and allows Mirana to escape. Meanwhile, in a dream, Slyrak reveals to Davion that The Eye that he is seeking, is inside Mirana herself and that she would need to awaken it in the throne room.

Davion and Slyrak join forces against Kashurra while Bram teleports Kaden to the battlefield with the portal scroll. Tihomir, who attempts to prevent Mirana from accessing the throne room, is killed by Asar. Kashurra reveals to Mirana that he is a dragon who has been transformed by the strange ore (just like Auroth), and has been drawn to Mirana due to her being the Eye of the Worldwyrm. He kills Marci and Mirana finally opens the Eye and kills Kashurra. Slyrak sets Davion free and Mirana is proclaimed Empress.

With the Eye opened, Slyrak traverses to Foulfell to confront Terrorblade and his army, as well as the souls of Uldorak and Lirrak, but he is killed as Terrorblade collect Slyrak's fiery spirit. Drysi, now hunted by the strengthened troops of Selemene's, allows Terrorblade to enter her body.

With Selemene's power taken away, Luna and the Dark Moon Legion gather the scattered troops around the enclaves and return with Nico to Mirana to join her Praetorian Guard. They are joined by Davion and Bram, who uncover that the dragons are converging to Broken's Peak, a sign that Slyrak has failed to kill Terrorblade and that Terrorblade is launching an assault on the Invoker.

As Mirana's group prepares, Kaden instructs Bram to stay and appoints him Father to rebuild Dragon's Hold. Entering Foulfell with the Invoker, Mirana, Davion, Luna and Kaden experienced traumatic flashbacks under the influence of Terrorblade. The Invoker conjures an invocation to summon Fymryn, now with the almighty strength of a goddess, who saves Empress Mirana's group from their flashbacks and joins the fight. The group mounts an all out assault on Terrorblade and his army, while Davion sacrifices himself to kill the demon.

Having her memory of the old world altered, Empress Mirana now rules Helio Imperium in the new world, with Marci, Lina, Emperor Zal, Shabarra and Tihomir resurrected and living in the new world. Informed of the appearance of a large red stone that has surfaced at Hinterlands and has turned the villagers there into monsters, Empress Mirana and her army burn down the village while bringing the stone back. Emperor Zal, who is suffering from dementia due to the loss of his wife, instructs Mirana to bring the stone to find the Oracle.

The Oracle reveals to her that it is a Direstone, which restores her memory of the old world. He explains that the Invoker has used the pillars of creation to collapse all realities into one. Deducing that since it is the pillars of creation which created the new world, Mirana plans to use it to restore the old one. Empress Mirana tells Lina and Luna to return to their father.

While traveling to Slyrak's cavern, Davion, Empress Mirana and Marci encountered Hellbear, a creature under the influence of the Stones, and a tree under the control of the Direstone. After destroying both, and unconvinced by Mirana's explanation, Davion leaves Empress Mirana and the alternate version of the mute Marci.

The Invoker falls into a healing sleep while Filomena revisits Mene, sensing that Mene's residual memories might provide answers. Filomena accesses Mene's mind and visits fragment memories of the old world as Fymryn. Piecing together the pieces and learning the existence of the two moons among many things, Mene gets her memories of her past life back and wakes the Invoker up, telling him to reveal the truth to Filomena.

Filomena discovered from the Archronicus that the second moon in the old world was what protected Earth from the Direstones and ores of the shattered Mad Moon. The Invoker confesses to Filomena that this is his twelve thousand-four hundred-and-third attempt to reshape the universe, and that without the second moon in the new world, the entire Earth except the Invoker's tower will eventually be destroyed.

Shabarra and Tihomir, now elected as regent and Viceroy, respectively, by the Senate, dispatch Lina and the army to repel attacks from the Coriel'Tauvi. After accepting a parley from general Drysi, commander of Principality, Lina assists the returning Mirana with Marci and Luna to take the throne back by force, while Emperor Zal dies from illness.

Following Emperor Zal's death, Empress Mirana opens "the Eye" of the Sun Goddess deep within her fully and ascends to goddess-like status and infinity powerful solar-based cosmic abilities. Filomena, with the help of her father, attempt to perform "the Forge", a procedure to remake the universe. The use of the dragons' souls during the procedure established a telepathic connection between Filomena and Davion.

Filomena suggests using the dragons' souls to bolster Arc Warden's power to buy time, but is rebuffed by the Invoker, stating that it will drain her life and awaken the Eldwyrms to wreck the Earth instead.

Fymryn, having recently fully bonded with Mene's dormant essence within her, whisks Empress Mirana from space, and tells her that she remembers the old world. The Invoker attempts to stop Filomena from conjuring The Forge, but is interrupted by Davion, who turns into Hybrion. The Invoker and Hybrion's confrontation concludes when Empress Mirana, Mene and Filomena appear and teleport Hybrion back to the Invoker's valley. Filomena confesses to her beloved father that she is inflicted with the exact same illness that had killed her as a girl in the old world, and they reconcile.

Filomena tells Empress Mirana that her divine spark, The Eye, would allow her to restore the old world. After bidding farewell to her allies, the Invoker and Filomena conjure The Forge with the dragon souls, returning Mirana to Foulfell of the old world, at the moment the Invoker attempts to rebuild the new world. With the Invoker's plan failed, Mirana and her allies leave the Invoker in Foulfell and return to Earth.

As they mourn the death of Davion who died fighting Terrorblade, Fymryn (now Mene) and Mirana agree to work together to restore the world. Mirana finds the Archronicus in the Invoker's Tower, and pass it to the shopkeeper for safekeeping, who accepts it as a "divine favor" from the human embodiment of the almighty Sun Goddess herself.