The game's name comes from the eponymous Ancients' Gates, which are the central focus of the story.
"There are legends from times long past, of an age without kings, when the world was united by an alliance between dragon and man. These are the legends of the Order of the Flame, when noble warriors soared on the winds, and great wonders were worked upon the world.
"Though the Order held strong for centuries, it was destroyed at last from within, brought low by the traitors of the Dark Union. War engulfed the world, and civilization crumbled. By the time the madness had ended, all had been laid to waste. The dragons of the Order, wounded in spirit, withdrew into timeless slumber to await a time when the virtues of the Order were honored once more. For mankind, the Fallen Age had begun.
"Centuries wore on. Evil grew ever stronger until the vile banner of the Dark Union was raised once more.
"It was then that the warrior, Rynn, discovered the resting place of the dragon, Arokh. Through the forgotten ritual of the Bond, their souls were joined as one, and the first faint spark of the Order was rekindled at last. Together, they took to the skies like a rising storm, driving back the forces of the Dark Union and ending their dreams of conquest. Victory was theirs, but it had come at a terrible cost.
"Rynn's village had been destroyed, and her younger brother, the last that remain of her family, had been lost. Saddened and weary, they returned to Rynn's village to search for any who might have survived.
"Little did they know, their struggles had only just begun."
- - The Book of Drakan
Having defeated Navaros and saved the world from the threat of a re-born Dark Union, Rynn and Arokh return to the ruins of her village. While Rynn buries the dead, Arokh travels up and down the valley, but finds no trace of anyone, not even the wartoks who destroyed everything. Rynn holds out hope that some of the villagers could still be alive in hiding, but Arokh knows that they are the only survivors of this dreadful attack.
Arokh cannot stay, however, as he says he has been hearing things: the Grand Summons of the Order. He senses it is coming from the North, where the city of Surdana once stood. Rynn wishes to join him, but must remain to bury the dead. They agree to meet in a few days, and Arokh departs for the North. A few days later Rynn departs and enters through the main gate into Surdana and is greeted by General Dehrimon, who informs her that Surdana's leader, Lady Myschala, is awaiting her arrival and that Arokh would meet them there shortly. Making her way through the mountains and battling Grull bandits Rynn arrives in Surdana's town center just in time to witness an attack by a Desert Lord. After killing a soldier the Desert Lord is banished by the Sorceress Jade, who reveals to Rynn that she was the one who called Rynn and Arokh to Surdana and explains Surdana's plight at the hands to the Desert Lords and concludes by inviting Rynn to her tower to learn magical spells. Rynn then goes to the palace and is greeted by the Royal Seer Zola Dane, who in turn points her in the direction of the throne room and Lady Myschala.
Myschala then reveals the reason why Rynn and Arokh were called to Surdana: Long ago there existed powerful beings called Spirit Dragons, believed to be the ancestors of the dragons of the Elder Breed. The most powerful of their number was the Dragon Mother, Mala Shae, and it was her who called all of the dragons to leave the world of Drakan after the Dark Wars. Now, however, there may be a way to contact the Dragon Mother and bring her and the rest of the dragons back into the world. In Surdana there exists a massive portal called the Mother's Eye that can connect with four other portals across the world. Furthermore when all of the portals are activated they can extend beyond the world to Mala Shae and the Spirit Dragons. To this day the portals remain closed but can reactivated by a dragon of the Elder Breed, hence the reason why they need Rynn and Arokh's help. Just as Myschala finishes recanting her story Arokh arrives and reports that he was unable to retrieve the Cypher Rune from the swamps of the Shadowmire. The Cypher Rune is an amulet that is necessary for Arokh to open the gates and asks Rynn to go in his place the Shadowmire to retrieve the Rune.
Rynn delves into the Shadowmire, battling her way through the frog-like Trogs. Along the way she rescues a farm girl named Semira and an amateur adventurer named Nicols from the Trogs (earning her the Earth Blade in the process) and, with the help of a hermit, makes her way into the roots of the Tree of Mourning where the Cypher Rune is waiting and kills the chief of the Trogs, Toad Fist. Upon exiting the Shadowmire she witnesses the leader of the Desert Lords, Jasaad Duthane, warning Myschala not to open the Ancient Gateways and commands that she and her people submit to the Desert Lords, otherwise they would face death. Rynn gives the Cypher Rune to Arokh, giving him the ability to open the gateways. They fly to the Andrellian Isles to look for a guide to take them to Ravenshold, where the first of the gateways is located.
The Andrellian Isles are caught in a perpetual storm created by a Grull Shaman named Bonegrinder, who has been given additional powers and allies by the Desert Lords. Rynn and Arokh save the men of the outpost from some Grull and their catapults. The men of the outpost tell Rynn about Master Sevoth, a wizard that has been aiding the men and keeping order, who is now dying from poison, and ask Rynn to retrieve his medicine pouch to save his life. She succeeds in retrieving Sevoth's medicine pouch and some ship charts from the Wartoks and return them to their owners. Sevoth tells Rynn more about Bonegrinder and offers to teach her some magic to combat him if she can retrieve some Mana Crystals from a nearby mine to replenish his power. Afterwards Rynn and Arokh make their way to Bonegrinder's base and are forced into combat with Mezzidrel, an enormous, two-headed sea serpent and survivor of the Dark Wars that Arokh once granted mercy but is now forced to kill. After defeating Mezzidrel Rynn enters Bonegrinder's base, making her way through Wartoks and confronts the shaman, warning him to lift the storms and allow the sailors to leave but he refuses, forcing Rynn to kill him. With Bonegrinder's death the storms clear and Rynn and Arokh follow the sailors to Ravenshold.
In Ravenshold they meet the Northmen, who point them in the direction of the first Gateway, which they open and reenter Surdana. They are then informed by Dehrimon that a Wartok Captain named Snotmaw has gathered the monster tribes to attack Surdana and ask them to kill Snotmaw in his headquarters to the south in Kragmoor to disrupt the alliances of monsters. While in Surdana Rynn also aids the people, such as clearing the catacombs of a monastery of undead, killing a Death Mage called the Inquisitor and even stopping the resurrection of a necromancer named Khossa Vole.
Rynn and Arokh return to Ravenshold where they are told by their leader that the Northmen are currently at war with another monster tribe called the Half-men to the North. The next Gateway is located in their territory in Shiverbane, but the Half-man (with the help of the Desert Lords) have barred the way into Shiverbane with a magical barrier. The chief of the North men tells Rynn to seek out Zeggoro the wizard for help. When Rynn meets with Zeggoro the wizard agrees to help since he also despises the Half-men but requires special ingredients for the spell needed to open the barrier: the Visionary Amethyst, the blood from a pagan alter, the ashes of a warrior fallen twice stirred with a blade of purest gold. Zeggoro tells Rynn to talk with one of the North men to get her started in finding the ashes of a warrior fallen. She meets with the blacksmith in Ravenshold, who informs her that his cousin Seborna was interested in entering a tomb where the ashes might be found. The blacksmith first asks Rynn to find out what happened to his cousin, who went into the hunting grounds of a massive yeti named Daemog. Rynn goes into the hunting grounds, kills Daemog and finds Seborna's journal next to his remains and brings the journal to the blacksmith. The blacksmith gives Rynn a key to the tomb, allowing Rynn to retrieve the warrior's ashes. While in Ravenshold she also acquires a vial of blood from a Grull camp, used in their pagan rituals. Rynn and Arokh then make their way further north, finding another human encampment in the Northern Tundra. Rynn questions the men there and finds out about a magic portal with "ice beasts". Rynn also meets Captain Serris who offers his gold sword if Rynn could retrieve the magic gauntlets used by the "vanishing Wartok" that has been robbing his men. Rynn enters the portal and battles her way through waves of Ice Golems and retrieves the Visionary Amethyst, a blue jewel, from the eye of a giant, deactivated Ice Golem. With all of the ingredients she returns to Zeggoro. While Zeggoro prepares the spell Rynn and the North men drive back the Half-men, allowing the wizard to dissipate the barrier.
Rynn and Arokh enter Shiverbane and battle their way into the compound, where Rynn is ambushed and captured, forcing her to find a way to escape and make her way through the compound relying only on her wits and magical skills. She is able to retrieve her gear and finally combat Maulgak, the leader of the Half-men, killing him in combat. Jasaad appears before Rynn and gives her the same warning he gave to Myschala to not open the gates and to surrender to the Desert Lords. Rynn and Arokh open the Gateway in Shiverbane and return to Surdana.
Rynn discovers that while they were away the palace was attacked from within by Jasaad's Soulless warriors. They find out that Zola Dane has betrayed Surdana to the Desert Lords. Rynn battles Zola and forces him to retreat, releasing Lady Myschala from his grasp. Rynn and Arokh chase Zola Dane into the Desert of Tears to the South where the last two Gateways are located. While in the desert, Rynn and Arokh rescue some local farmers from an attack of undead Bone Dragons. The farmers inform Rynn that the last Gateway has been transported up into Stratros, the Desert Lords' fortress in the sky. The farmers also ask Rynn to rescue the young boy named Perry, who was captured by the Wartoks. When Rynn rescues Perry, he reveals to her that the reason why he was captured was because the undead have been active in the old ruins, causing some of the old traps in the ruins to activate and killing some Wartoks, making them believe that Perry was responsible. Rynn escorts Perry home safely, who in turn give Rynn a key into the Devil's Mouth Ruins. Arriving at the ruins Rynn and Arokh are greeted by Zola Dane, who uses his magic to awaken two dragons, Shaza and Tora, from their stone slumber. Shaza and Tora bear a personal grudge against Arokh and attack, forcing Rynn and Arokh to fight and kill them. Rynn enters the ruins and battles the undead under the command of Gothraul, the prince of ghouls and former member of the Dark Union. Rynn deactivates the traps, allowing Arokh entrance into the ruins. Just as Rynn finds the elevator that would take her and Arokh into Stratos she is attacked by Zola Dane but she is able to kill him. Both dragon and rider board the elevator and rise into the sky towards Stratos.
Upon arriving in Stratos Rynn and Arokh are greeted by a slave named Mardis, who tells them where the last Gateway they need to open is located, however warns them that the Pain Golem, the most powerful servant of the Desert Lords, has been placed in charge of guarding the Gateway. The Pain Golem is almost indestructible and only its creator, Yutaji the Flesh Mage, knows the golem's weakness, however Mardis warns Rynn not to visit the Flesh Mage because he has gone insane and even the Desert Lords fear him. Mardis does tell Rynn of how to gain entry into Yutaji's palace where he has been sealed up by going to the ferry where slaves are transported to the palace. Rynn and Arokh battle through swarms of evil dragons, griffins, Desert Lords and Soulless warriors. They arrive at the Bridal Hall, where the Ferry to the Flesh Mage's palace, the Necropolis, arrives. The gatekeeper warns Rynn not to enter because the Bridal Hall has an enchantment on it that destroys the will of all who enter, this keeps the minds of the slaves sedated so that they don't resist. Only the workers are immune because of an antidote that a Djinn named Grotus brews for them. Rynn enters Grotus' lair and claims a vial of the antidote for herself and kills Grotus in the process. She returns to the Bridal Hall and drinks the antidote, allowing her to enter the hall safely and board the ferry to the Necropolis. The slave operating the ferry warns Rynn that there is no reasoning with the Flesh Mage because his mind is gone and that the only way to kill him is to destroy the urn that his soul is encased in. Upon entering the Necropolis she meets the Flesh Mage, a psychotic creature that wears the skins of his female victims like a robe. The mage chases Rynn through the palace, while she is also hounded by the mage's golems and the undead. When Rynn reaches the balcony, she causes the chandelier to fall on the alter where slaves are sacrificed to the mage, destroying both and revealing the soul urn to be encased beneath. Rynn destroys the urn and thereby killing the Flesh Mage. Yutaji's spirit, now free from the urn and from the madness that plagued him, apologizes to Rynn, explaining that Jasadd had cast a spell on him to drive him mad. To make up for his misdeeds Yutaji bequeathes the Golem Staff to Rynn, a weapon that can kill the Golem, and asks Rynn to released the last small portion of his soul within the golem so his soul can rest in peace. Rynn returns to the palace where the Pain Golem is guarding the last Gateway and uses the Golem Staff to deactivate the Golem. Jasaad arrives, furious at Rynn for foiling his plans. Rynn warns Jasaad to leave Drakan while he still can but Jasaad instead attacks Rynn. Rynn is able to weaken Jasaad but in a last gambit Jasaad uses the Golem Staff to combine his power with the Pain Golem. Arokh arrives just in time for him and Rynn to battle Jasaad and the Pain Golem. By attacking Jasaad, who is being held in the Pain Golem's clutches, Arokh is able to weaken the Golem, causing it to drop Jasaad and collapse on top of him, killing the leader of the Desert Lords.
The game concludes witha reading from the Book of Drakan, similar to the prologue.