After more than a year of training under Peter Parker, Miles Morales has mastered his superpowers and established himself as the original Spider-Man's crime-fighting partner, though he still struggles to adapt into his new role. While he and Peter escort a police transport carrying prisoners to the rebuilt Raft, Miles accidentally releases several inmates, including Rhino. While trying to stop Rhino's rampage through the city, Peter is knocked unconscious. Miles intervenes to protect him and defeats Rhino with his new bio-electric ability, later dubbed "Venom". Leaving Rhino in the custody of energy corporation Roxxon, headed by Simon Krieger, Peter informs Miles that he will be going to Symkaria for a few weeks to assist Mary Jane as her photographer as she does her story on the country's civil war, and entrusts Miles to look after New York in his absence as its sole Spider-Man.
It features the same open world, a fictionalized version of modern-day Manhattan, which is covered in snow because the game is set during Christmas. Miles controls similarly to Peter Parker, but with new animations and abilities, which are unlocked as the storyline progresses. The new powers include Venom Blast, which allows the player to incapacitate enemies with bio-electricity, and charge or drain electronics; Camouflage, which gives Miles temporary invisibility; and Mega Venom Blast, consisting of a massive explosion of bio-electricity that damages all nearby enemies. The game introduces new gadgets, such as Remote Mines, which can attach to enemies or electrical panels; a device that summons holographic fighters to help in combat; and Gravity Wells that trap multiple enemies and make them easier to hit. Miles' abilities and gadgets can be upgraded as the player levels up via a skill tree system. Another feature that the game offers is Miles' Spider-Man app which gives him feedback on crimes happening in New York City and the location of these crimes. It informs the player of any side missions that are available for them to complete, which is beneficial to level up.