The legendary Tower of Druaga is resurrected eighty years after the hero Gilgamesh has taken it down. In order to destroy the evil deity Druaga, the Kingdom of Uruk dispatches its troops to the tower, but the expedition repeatedly fails in its efforts. A young man named Jil who has been blessed by the goddess Ishtar, is awarded a set of brilliant golden amour and a sword from Gilgamesh as tokens to defeat the maumet. Sent off by the cheering crowd, our young hero Jil confidently sets out to confront the evil deity inhabiting the tower. Helped by great friends such as the archer Neeba and a Mage called Fatina, he heads for the uppermost floor of the Tower!

Because of a blunder during his first battle, Neeba is forced to fire Jil from the group. Though disheartened by the humiliating dismissal, his desire to conquer the evil deity does not wane. As Jil wanders the city of Meskia which is filled with anticipation for the third season of expedition to the Tower, he meets a mysterious girl named Kaaya and a close-mouthed young woman called Ahmey. When Jil learns of the great hero King Gilgamesh's visit to the city, he takes his new friends to watch the procession. There he accidentally comes upon the figure of Neeba in the bustling crowd.

Jil barely escapes from the scene of the King's assassination thanks to the quick-wit of Neeba. The next day, the review of troops by the King goes on as scheduled. At the ceremony, Jil is dumbstruck; before him is none other than King Gilgamesh who he saw murdered the night before! Meanwhile in the city of Meskia, a giant slime that suddenly appeared was causing much havoc. A young girl named Coopa is embodied by the slime but is quickly rescued by Ahmey. When Coopa learns that Jil and the others are "Climbers", she insists on allowing herself and her master, a mage named Melt, to joint their party.

Jil and his party set out on their expedition among the other Climbers and face their first battle. However, their struggle against the powerful foe Kusarakk is harder then they had expected as their teamwork has not yet been refined to say the least. Ahmey is the only member who has experience as a Climber and they follow her confident guidance. They listen to her advice regarding battle strategies and numerous rules of thumb about Climbing. Now equipped with the necessary knowledge and skills, they resume to confront the Kusarakk again.

On their journey Jil and the others pass a signboard indicating a shortcut. But the "shortcut" turns out to be a series of different traps that hinder their efforts to go forward. While one of the traps causes their gender to switch, the other forces them to wear animal costumes. Subsequently they arrive at the final gate. But getting through that exit door turns out to be harder they had ever imagined!

Jil and his party encounter another party that has practically been wiped out in a fierce battle against the ogres. There they manage to rescue an aged warrior called Gigi who was an acclaimed Guardian of the past. They take Gigi to a camping area on the way but are unable to take a moment of rest as they are plagued by one jam after another. One of the party members has a wallet pick-pocketed while a heated argument erupts between Coopa and Melt. In the end, reconciliation seems out of the question as Coopa, disgusted by her petulant master, decides to leave the party to be on her own!

The Uruk Army led by General Kelb is unable to move forward as a single-winged dragon suddenly appears before them. Inside the Tower, there is an unprecedented militant atmosphere as the Uruk Army's anger reaches a crescendo at the total annihilation of the Scout Regiment by the dragon. Jil's party and Neeba's party observe the army as they prepare for the upcoming battle against the dragon. Jil tries to persuade Neeba, who is also known by some as "Neeba the Dragon Slayer", that the Climbers need to work closely with the Uruk Army to defeat the dragon. Will he succeed in getting his party and Neeba's party to join the Uruk Army in their quest to slay the dragon...?

Kaaya is stricken by some unknown illness. The party is puzzled by this illness whose name and symptoms seem rather sketchy. Jil, in all his naïveté, sets out to search for the cause of this mysterious ailment. They finally arrive where the answer supposedly lies. Only, the place turns out to be nothing like any other floor in the Tower they have visited so far! What are the challenges that await Jil and his friends in this strange and unknown area?

Jil and his party enter an area supported only by thin pillars. They engage in a battle against a balloon-shaped monster called Barbar and, demonstrating well-coordinated team play, they defeat the enemy in the end, thanks to Melt's magical tricks. The festive mood from the victory, however, is short-lived as the feebly structured area collapses due to the explosion caused by Barbar's demise. The collapse of the area also extends to other areas on the same floor, thus causing Neeba's party and the Uruk Army much chaos. In the end, members of all parties find themselves separated from each other.

Jil’s party has now reached the “Shrine of Diamond”. The top floor and their ultimate goal “Shrine of Sky” is now close at hand. Neeba’s party, the Uruk Army and Pazuz go their separate ways in order to reach the top of the Tower. As the respective parties continue their quests, each and every Climber’s dreams, objectives and ambitions are intermingled and eventually develop into a fierce battle, marking another chapter in the history of the Tower of demon god.

The evil deity Druaga finally shows its gigantic figure. Neeba and his party bravely face off against it, but the demon god's power is so overwhelming that the party soon begins to loose ground. Seeing that they are cornered, Jil tries to rush to their rescue. However, he is stopped by Kaaya who maintains that they should continue to make their way toward the top floor of the tower. Jil shakes free from her grasp and dashes off toward Druaga...

The final installment of The Tower of Druaga. Jil must lead the surviving Climbers to defeat Druaga, and devises a strategy to lure him into the secluded small area at the top, where he would no longer be able to move as freely. Deciding to fulfill his calling as a Guardian, Jil volunteers to be the decoy and draw him in. Kaaya, seeing Jil risking his life for the sake of this mission, apologizes for things she cannot reveal.