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In Ultimate Spider-Man, the player can experience a free-roaming city environment that covers Manhattan and Queens. The player starts in story-mode where the game automatically switches between Spider-Man and Venom. Spider-Man travels by web swinging, but the player must shoot a web at an actual building to swing, much like in the previous game, Spider-Man 2. Spider-Man uses acrobatic attacks. Venom travels by using his symbiote to pull himself and by performing massive jumps. Venom attacks using his claws and tendrils. Venom can also throw cars at targets and perform much more brutal attacks, including eating people in order to gain health.

As the game progresses, Parker/Spider-Man and the player will have certain "City Goals" to accomplish in order to continue the storyline. There are additional activities throughout the game such as finding secret tokens, landmark tokens, comic book covers, and competing in trick races.

Spider-Man plays similarly to his Spider-Man 2 incarnation, using web shots as his main method of transportation and combat, while Venom has to resort to jumping for long distances. Venom's attacks are also generally stronger than Spider-Man's. Venom (like Spider-Man) can also scale buildings. Venom (as previously stated) can also leech life from enemies and civilians. The player has to do this constantly, as Venom's health is continuously depleting, even when he is not being attacked (the suit is feeding on Eddie Brock, so Eddie uses other people to feed it instead).