The core gameplay of Marvel's Spider-Man: Miles Morales is the same of its predecessor. It features the same open-world, a fictionalized version of modern-day Manhattan, which is covered in snow because the game is set during the holidays. Miles controls almost identically to Peter Parker, but with new animations and abilities, which are unlocked as the storyline progresses. The powers introduced consist of 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 also introduces new gadgets, including 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.
Like Peter, Miles possesses a "spider-sense", which warns the player of incoming attacks and allows them to dodge and retaliate, and web-shooters, which fire lines of webs that can be used during both traversal and combat, in several different ways. Miles can also jump, stick to surfaces, and fast travel using the New York City Subway system. Side-missions have been significantly altered, and are now accessed from an in-game phone app. Miles has several unlockable suits, some of which are based on existing versions of the character in media, as well as original suits created for the game. Many of these enhance Miles' abilities, such as allowing him to take less damage, stay invisible for a longer time, or regenerate Venom Power faster. During certain sections of the game, players control Miles in his civilian persona and cannot use any of his abilities or gadgets.