Ratchet and Clank Future: Quest for Booty offers a distinct experience where there is a greater emphasis on puzzle solving and platforming, introducing new elements such as Omniwrench Millennium 12's ability to manipulate objects. Moreover, Ratchet gains the ability to wield heliobrute, illuminating dark areas when needed. Omniwrench Millennium 12 also has a snap feature that allows you to manipulate strategic objects.

Familiar arsenal such as Combuster, Fusion Grenade, Nano Swarmers and others from Tools of Destruction return, providing a range of powerful tools. The story takes place one year after the defeat of Emperor Tachyon and the mysterious kidnapping of Clank by the mysterious Zoni, as shown in Instruments of Destruction. Ratchet and his partner Talvin Apogi receive vital information from the supercomputer IRIS, pointing them to Captain Angstrom Darkwater, a legendary space pirate with the knowledge to reach the Zoni.

The journey takes them to Darkwater's home planet, Murdegrow, in the Drogol sector. Sneaking aboard a pirate fleet hovering over the Sea of ​​Azores, their presence is quickly discovered, resulting in their capture by Sprocket, Darkwater's resourceful first mate. Shockingly, Sprocket reveals Darkwater's long-gone status. As a result of Rusty's timely intervention, Pete, masquerading as Captain Romulus Slag (previously defeated by Ratchet), changes their fate by ordering them exiled to the island of Hulefar.