The story recommences with teenager Miles Morales, now more confident in his role as Spider-Man after the events of the first film. His life, though still a complicated blend of high school demands and superhero duties, is thrown into disarray when Gwen Stacy, the Spider-Woman from another dimension, reappears, opening the gateway to the multiverse once again. Miles finds himself swept up in an even broader adventure that stretches the limits of what he understands about the Spider-Verse. As he travels through different dimensions, he meets a diverse array of Spider-People, each with their unique abilities, challenges, and perspectives on what it means to be a hero.

The journey through the multiverse isn't just a spectacle of vibrant new worlds and characters; it's also a test of Miles's resolve and an exploration of his identity not only as Spider-Man but as a son, friend, and individual. The complex dynamics of his personal relationships from his home dimension are juxtaposed with the exciting and sometimes chaotic alliances he forms with other Spider-People. A new threat emerges that challenges the very fabric of the multiverse, forcing Miles and his multidimensional counterparts to confront the possibility that their combined powers might still not be enough to save their interconnected realities from impending doom.