The story unfolds with the first king of Aurea, who attempts a futile attack on a dragon (voiced by Shohreh Aghdashloo) that has long plagued his realm. All of his men are slaughtered, leaving him at the mercy of the vicious creature.
Fast forward centuries later, we meet Elodie (Millie Bobby Brown), the young daughter of Lord Bayford (Ray Winstone). In a twist of fate, she receives a marriage proposal from Queen Isabelle (Robin Wright), who seeks to solidify her family's power through a union with her son, Prince Henry (Nick Robinson). To reinforce their struggling kingdom, King Roderick (Milo Twomey) sends ships laden with gold to seal this alliance.
Upon her father's insistence, Elodie accepts the proposal to assist their impoverished people. Lord Bayford expresses concerns that their homeland encounters brutal winters, and without substantial help, survival until summer seems bleak. Floria (Brooke Carter), Elodie's younger sister, joins them on their journey to Aurea.
As they arrive, the Bayford family is mesmerized by the riches and elegance of Aurea. Yet, from her chambers, Elodie spots a flickering flame on a nearby mountain, stirring her curiosity. Initially, Elodie and Prince Henry show little interest in one another, but their shared longing for adventure fosters a budding connection.
In the shadows, Lord Bayford discusses terms with the Queen, who offers him a staggering sum of gold. However, it is evident that his mind is troubled upon exiting their private meeting. Meanwhile, Lady Bayford (Angela Bassett) struggles to establish rapport with Queen Isabelle, who snubs her by referencing her humble origins, stating she is merely the daughter of a rope maker, lacking royal lineage. Isabelle underscores that this union is purely transactional: she needs a bride, and the Bayfords require financial aid. She even mistakenly calls Elodie "Eloise," showcasing her disdain.
Despite her stepmother's desperate pleas to rescind the engagement, Elodie complies, knowing its implications. Following a ceremonial wedding the next day, she and Henry participate in an ancient ritual in the mountains celebrated to honor their union. Queen Isabelle recounts the tragic history between the first king and the dragon that wreaked havoc upon their villages, detailing the terrible bargain made: the king sacrificed his daughters to quell the dragon's wrath.
As part of the ritual, Elodie and Henry's hands are cut and bound together, after which Henry throws her into the dragon's lair, believing it to be a customary ordeal. Upon awakening from the fall, Elodie realizes her designated fate as a sacrifice, her cries summoning the dragon, who is misled into believing she belongs to the royal Aurean lineage due to the mingling of their blood during the ceremony.
Elodie narrowly escapes the dragon's flames and discovers an enchanted cave illuminated by glowing slugs, which she gathers as a source of light. Inside, she unearths a haunting inscription, “Safe Here She Cannot Reach,” listing the names of prior victims and a map etched into the wall. While she sleeps beneath the healing glow of the slugs, her burn is alleviated.
However, her hope dwindles as the map leads her to a treacherous vertical drop, deepening her despair. She uncovers remnants of dragon hatchlings, revealing the cause of the royal sacrifices: the first king had slain three hatchlings, inciting the dragon's wrath. In a stirring moment, a rescue party led by her father arrives, but when confronted, he confesses his betrayal of Elodie for gold and the welfare of their people, which the dragon avenges by killing him.
Seizing the opportunity amidst the chaos, Elodie escapes the mountain on a horse, hiding from the dragon's fiery pursuit. Meanwhile, the failed sacrifice compels Isabelle to kidnap Floria as a new offering. Learning of this, Elodie returns to the mountain, confronting the dragon and attempting to plead her case, asserting they had been misled by the Aureans.
In a moment of clever strategy, Elodie tricks the dragon into harming itself, effectively gaining its trust. Once she proves her worth, she confronts the royal household during another arranged marriage, exposing their deceitful ways. Elodie warns the bride and her family to flee before the dragon unleashes its vengeance, resulting in the royal palace burning down with all inside.
Ultimately, Elodie, Floria, and Lady Bayford sail back home, empowered and adorned with supplies, accompanied by their newfound ally—the dragon—signifying a transformative journey that reshapes their fate.
