Full story
On Earth-65, Gwen Stacy is alone. Her world's Peter Parker turned into the Lizard and died fighting Spider-Woman, and everyone thinks she killed him. Her father, Captain George Stacy, is hunting Spider-Woman without knowing who she is. When Gwen unmasks in front of him, he points his gun at her. Right then Miguel O'Hara, Spider-Man 2099, and Jessica Drew show up. They belong to the Spider-Society, a team of heroes from across the multiverse, and they invite Gwen to join.
On Earth-1610, a year and a half after the first film, Miles Morales is juggling school, the suit and his parents. He's late for everything, including the party where his dad, Jefferson, is about to be promoted to captain. Along the way he fights the Spot, an Alchemax scientist whose body was turned into portal holes when the first film's collider blew. The villain blames Miles for his tragedy. Gwen drops in for a visit, the two spend a night together, and Miles secretly follows her through a portal to Mumbattan, Earth-50101.
There, the Spot drains the local collider's power. Miles meets Pavitr Prabhakar, that Earth's Spider-Man, and Hobie Brown, Spider-Punk. Against Miguel's orders, he saves Earth-50101's police captain. The result is a hole that nearly swallows that universe. At Spider-Society headquarters, Miguel explains canon events: fixed moments in every Spider-Person's life, like the death of a police captain close to them. Changing one wrecks the whole world. Miles realizes his dad is about to die.
Miles refuses to accept it and runs. Every Spider-Person in the building chases him. Miguel then drops the hardest part: the spider that bit Miles came from another universe, so Miles was never supposed to be Spider-Man. To Miguel, he's an anomaly, the original glitch that shook the whole web of universes. Miles escapes through a portal with help from Margo Kess, but lands in the wrong universe: Earth-42, where the spider came from.
On that Earth, Jefferson is dead and Uncle Aaron is alive. That reality's Prowler is Miles himself, a version who never became Spider-Man, and he captures the visitor. On Earth-65, Gwen tells her dad the truth, and he quits the force and takes her side. Kicked out of the Society, she gathers Peter B. Parker, Pavitr, Hobie, Margo, Spider-Ham, Spider-Man Noir and Peni Parker to rescue Miles. The Spot is ready to strike Miles's Earth. The film ends with none of it resolved.