In Pirates of the Caribbean: At World's End, Captain Davy Jones now serves Lord Cutler Beckett, who possesses Jones' heart and forcibly controls him and the Flying Dutchman, which is first seen rising from the sea, mercilessly destroying pirate ships with its powerful cannons. This irritates Lord Beckett who wants survivors to interrogate, so to ensure Jones does as he is ordered to. Beckett places Admiral James Norrington and a squad of East India Trading company marines and the Dead Man's chest placed on board as well to remind Jones he is under their control. The Dutchman accompanies Beckett's flagship, Endeavour in its mission to eradicate piracy. When the Dutchman attacks Sao Feng's ship, the Empress, it takes its crew captive (including Elizabeth Swann who is made captain by the dying Sao Feng). Elizabeth and her crew escape the Dutchman with Admiral Norrington's help, although he is killed by a deranged Bootstrap Bill Turner. Jones and his crew attempt a mutiny against the East India Trading Company marines stationed on board, but Mr. Mercer, Beckett's henchman, proclaims the ship is under his command, temporarily subduing the uprising.
The Dutchman leads the East India Trading Company armada in battle against the Brethren Court. The Dutchman and the Black Pearl engage in battle while entering a monstrous maelstrom (caused by Calypso, Jones' ex-lover). Jones is killed when, aided by Sparrow, the mortally wounded Will Turner stabs Jones' heart, and Jones falls off board into the maelstrom. The Dutchman is also sucked into the maelstrom as Swann and Sparrow escape. The Dutchman 's crew carve out the now-dead Will Turner's heart (as whoever kills the Dutchman's captain must replace him) and place it in the Dead Man's Chest. The Dutchman re-emerges from the maelstrom with Captain Will Turner at the helm. Joining forces with the Pearl, the two ships face off against the Endeavour. Stunned by this unexpected alliance, Beckett is unable to respond, and his crew abandons ship just as the Endeavour is being destroyed and Beckett is killed.
The Dutchman 's crew revert to human form and the ship reverts to its original form as well, and Will and Elizabeth meet on an island and consummate their marriage. Will departs at sunset to fulfill his destiny as the Dutchman's captain, leaving his disembodied heart in Elizabeth's care. Will frees Bootstrap Bill from his servitude, but Bootstrap decides to remain with his son as part of his new crew. Following the end credits: ten years later, the Dutchman reappears upon the horizon amid a green flash as Elizabeth and her son await its arrival. And as sun sets, he is seen with the ship.