Ashitaka is the protagonist of the story, introduced as the last prince of the Emishi, a reclusive tribe in the northeast. His life is permanently altered when a boar god transformed into a demon of hatred, a Tatari-gami, attacks his village. In the act of defending his people, Ashitaka kills the demon but is afflicted by its curse, which brands his right arm with a living, painful mark that will eventually spread through his body and kill him. The wise woman of his village explains that the demon came from the west, so Ashitaka cuts off his topknot, signifying his exile, and departs on his loyal red elk, Yakul, to find the source of the corruption in the hopes of lifting his curse. His journey is framed by the elder's parting advice: to go forth and "see with eyes unclouded by hate."

Ashitaka's personality is defined by a profound sense of calm and duty, which masks a deep well of sorrow and anger that is dangerously fed by his curse. He is fundamentally kind, self-sacrificing, and possesses a quiet humor, as seen in his gentle interactions with the women of Iron Town and his deadpan remarks to the forest spirits. Despite being a supremely skilled warrior, he is a pacifist at heart who always seeks a peaceful resolution and tries to reason with his opponents before resorting to violence. His core motivation is not revenge or a simple cure for himself, but to understand the chain of hatred that turned a god into a demon. He is driven by a desire to end the cycle of violence between humans and the forest gods, even as the corruption on his arm pulses with the demon's own fury, tempting him to give in to his darkest impulses. He exercises immense restraint, forcing his cursed arm to obey his will, using its supernatural strength only to protect or to end a conflict, rather than to feed the hatred that created it.

His role in the narrative is that of a mediator and an outsider. Arriving in the west, he finds himself caught between two uncompromising factions: the industrial Iron Town, led by the pragmatic Lady Eboshi, and the gods of the ancient forest, led by the wolf goddess Moro and her human-raised daughter, San. Ashitaka refuses to side entirely with either, seeing the suffering and righteousness on both sides. He recognizes that Lady Eboshi provides a home for lepers and former prostitutes, empowering the marginalized, but at the terrible cost of destroying the forest and its gods. Conversely, he understands San and the wolves' fight for survival, but sees that their pure hatred cannot stop the march of human industry. This places him at the center of every major conflict, from protecting Iron Town from samurai raiders to physically breaking up the final battle between San and Lady Eboshi. He is the only character who actively attempts to stop the war rather than win it.

Ashitaka's key relationships drive his development. His connection with San is immediate and profound; upon first seeing her, he is struck not by her ferocity as the "Princess Mononoke," but by her beauty and tragic strength. He repeatedly risks his life for her, earning her trust and affection despite her deep-seated hatred for his kind. Their bond is a tentative bridge between two worlds, but the film concludes with them accepting that they cannot live in each other's worlds, only meet in the space between. His relationship with Lady Eboshi is one of respectful opposition; he saves her life and acknowledges her good qualities while directly confronting her destructive ambition. His most constant companion is Yakul, his elk, whose unwavering loyalty symbolizes the peaceful coexistence with nature that Ashitaka strives for. His development is not a traditional arc of personal change but rather a deepening of his resolve. He enters as an exile with a death sentence and grows into a figure of decisive action, choosing to live not by succumbing to hatred, but by forging a new path of understanding. He is healed not by the destruction of his enemies, but by the restoration of balance when he and San return the Forest Spirit's head, an act of pure selflessness.

Ashitaka's notable abilities are formidable, and they are divided between his natural skills and the power of his curse. Before being cursed, he was already the greatest warrior of his tribe, a master archer and swordsman. He demonstrates incredible accuracy, even while riding at full speed, as shown when he shoots the demon boar through the eye. After being cursed, his right arm gains a demonic, supernatural strength that is both a gift and a peril. He uses this power to fire arrows with enough force to sever the arms and heads of samurai, to lift the immense portcullis gate of Iron Town single-handedly, and to catch a flying arrow mid-air and shoot it back at his opponent. However, this power is directly linked to his anger; when he gives in to rage, the curse grows and threatens to consume him. His greatest ability, therefore, is not his physical prowess but his unbreakable willpower, which allows him to control the curse, refuse its violent urges, and maintain his pacifist principles even when facing overwhelming cruelty and his own impending death.