Players assume the role of Daxter in his role as a bug exterminator, while he is searching for his friend Jak throughout the game's story. Daxter can perform double jumping and ledge grabbing, can crouch to squeeze through narrow gaps, make use of trampolines to reach higher ledges and ride on ziplines, and make use of vehicles to move around the game world's map. Portals and gateways are encountered within the main environment which lead to locations containing missions that players must complete in order to advance the story.
Combat in the game focuses mainly on melee attacks using an electronic blue eco powered bug-swatter, with players able to perform combo attacks on multiple enemies. After the initial missions, the player gains access to an extermination tank which sprays green eco-based bug spray to stun enemies, with it later able to be upgraded with several new functions, including a jet pack to allow Daxter to fly, a flamethrower modification which can improve the effectiveness of the jet pack, and an ultrasonic attachment that shoots blue eco-based high radial damage projectiles. Damage taken from enemies and certain environmental hazards can be recovered by collecting green eco health packs, while the spray tank's supply can be regenerated by absorbing green eco clusters.
Two forms of collectibles can be found during the game, including Golden Bug-Gems, similar to the Metalhead Gems from the second and third installment of the Jak and Daxter series, along with the traditional Precursor Orbs, the latter of which can be used to unlock special features. In addition, players can unlock unique items by breaking picture frames found hidden throughout the game, and with a Jak X game connected to Daxter, can alter the character's goggles and, if the connected save file is 100% complete, a modified Hover Scooter paint scheme.