For centuries, sea beasts have emerged from the depths, wreaking havoc on humanity. To combat these formidable creatures, crews of hunters set sail on their ships, the most renowned being the crew of the Inevitable, helmed by the legendary Captain Crow, his first mate Sarah Sharpe, and his adopted son and boatswain Jacob Holland. Their successful hunts have garnered the support of the King and Queen through the Three Bridges Society, a testament to their prowess over the years. However, after a near-fatal encounter with a beast, Crow reveals to Jacob that he plans to make him captain once they defeat the elusive creature known as the "Red Bluster," which had taken Crow's left eye long ago.
Upon returning to Three Bridges to collect their reward, the crew learns that they are to be replaced by the modern naval vessel Emperor, commanded by Admiral Hornagold. This news infuriates Crow and Sarah, sparking a heated confrontation that nearly leads to their arrest. In a bid to prove their worth, Jacob proposes a final challenge: to hunt the Red Bluster, which Admiral Hornagold agrees to, leading to a competition between the crews of the Inevitable and the Emperor.
During their voyage, the crew stumbles upon an orphan girl named Maisie Brumble, who has snuck aboard, inspired by the legacy of her late hunter parents. As they pursue the Red Bluster, a moment of crisis arises when the ship faces destruction. Against Crow’s orders, Jacob reluctantly allows Maisie to free the Bluster, saving the crew but risking their exposure to the ocean. Both Jacob and Maisie subsequently find themselves swallowed by the very beast they sought to conquer.
Stranded on a remote island inhabited by various sea beasts, Maisie befriends the Bluster, whom she affectionately names Red, and develops a bond with a smaller beast named Blue. As she fosters a belief that these creatures are misunderstood, Jacob initially resists this notion. Together, they persuade Red to carry them to Rum Pepper Island, hoping to secure a way back to Three Bridges.
Meanwhile, believing Jacob to be dead, a heartbroken Crow seeks the famed hunter and trader Gwen Batterbie, who provides him with a poison-tipped harpoon potent enough to slay Red. As Jacob and Maisie traverse the island on Red's back, they grow closer, with Jacob starting to share Maisie's sentiment that the beasts are innocent beings rather than threats. Upon reaching Rum Pepper Island, they encounter Admiral Hornagold, who is in position to attack them.
As Red retaliates against the Imperator, a scuffle ensues, resulting in Maisie being wounded. Jacob manages to stop Red’s rampage at great personal risk, only for Crow to take action that could endanger both Maisie and Red. While being nursed back to health, Maisie is imprisoned aboard the Inevitable, which soon returns to Three Bridges with Red captured.
After a daring escape initiated by Blue, Maisie uncovers the truth: the Crown’s narrative of sea beasts is a fabrication designed to maintain their power. As Crow prepares to execute Red publicly, Jacob intervenes, leading to a confrontation between him and Crow. With the help of Maisie and Sarah—who begins to see the truth of the beasts as Maisie has—they free Red from captivity. In an unexpected turn of events, they manage to convince Red to spare Crow’s life, exposing the Crown’s deceit to the public.
Witnessing the gentle nature of the creatures, Crow and the populace of the kingdom renounce their long-held beliefs. With Red and the other sea beasts finally free, Maisie, Jacob, and Blue embark on a new chapter of their lives, united as a family and ready to embrace the future.
