The best spider-man film. Beyond being funny, creative, and wonderfully animated, it truly has an understanding of the character of Spider-Man.

New York City teenager Miles Morales struggles to live up to the expectations of his father, police officer Jefferson Davis, who sees Spider-Man as a menace. Miles adjusts to prep school, and visits his uncle Aaron Davis, who takes him to an abandoned subway station to paint graffiti. Miles is bitten by a radioactive spider and gains spider-like abilities similar to Spider-Man.

Returning to the station, Miles discovers a collider built by Wilson Fisk, who hopes to access parallel universes to bring back his late wife and son, whose deaths he blames on Spider-Man. Miles watches as Spider-Man attempts to disable the collider while fighting Wilson's henchmen, Green Goblin and the Prowler. Spider-Man saves Miles, but Green Goblin shoves Spider-Man into the collider, causing an explosion that severely wounds Spider-Man. Spider-Man gives Miles a USB flash drive designed to disable the collider, warning that the machine could destroy the city if reactivated. After watching in horror as Wilson kills Spider-Man, Miles flees with Prowler in pursuit, eventually getting away.

As the city mourns Spider-Man's death, Miles tries to honor his legacy and become the new Spider-Man. While trying out his newfound abilities, he inadvertently damages the drive. At Spider-Man's grave, Miles meets Peter B. Parker, an older and worn-down version of Spider-Man from another dimension. Upon meeting him, Miles discovers his ability to emit bio-electric bursts called "venom-blasts". Peter reluctantly agrees to train Miles in exchange for help stealing data to create a new drive. They infiltrate Wilson's research facility, and Miles discovers he has the power to turn invisible. They are confronted by mad scientist Olivia Octavius, who discovers that Peter will die from cellular decay if he remains in their dimension.

Chased through the laboratory and surrounding forest by Octavius, Miles and Peter are saved by Gwen Stacy, a Spider-Woman from another dimension. They then visit Peter's aunt, May Parker, who is sheltering more Spider-people from other dimensions – Spider-Man Noir, Peni Parker, and Spider-Ham – who are also deteriorating. Miles offers to disable the collider so the others can return home, but after questioning and testing him, they tell him that he lacks experience. Distraught, Miles retreats to Aaron's home, where he discovers Aaron is indeed the Prowler. Miles returns to May's house, where Peni has completed the new drive; he is followed by Wilson, Prowler, Octavius, Scorpion, and Tombstone. In the ensuing brawl, Miles reveals his identity to Aaron just as Aaron corners him. Unwilling to kill his own nephew, Aaron spares Miles, but is fatally shot by Wilson. Miles flees with Aaron, who tells him to keep going before dying. Jefferson arrives on the scene and Miles escapes, leading Jefferson to mistake Miles as Aaron's murderer.

The heroes regroup with an distraught Miles at his dorm room. Peter restrains Miles to ensure his safety and leaves with the others, choosing to sacrifice himself by staying behind and deactivating the collider. Jefferson arrives outside Miles' door and, assuming Miles does not want to speak to him, apologizes for his mistakes and inspires Miles. Miles then manages to control his powers, escapes his restraints, and creates his own Spider-Man suit with May's help. He joins the heroes, defeating Wilson's enforcers and using the new drive to send them home. Wilson fights Miles, attracting the attention of Jefferson, who realizes that Miles is on his side. Jefferson encourages Miles, who subdues Wilson with his venom-blast and throws him at the kill switch, destroying the collider.

Wilson Fisk and his henchmen are arrested for their crimes and Jefferson recognizes the new Spider-Man as a hero while receiving evidence of Wilson's murders of Spider-Man and Aaron. Miles embraces the responsibilities of his new life, while the heroes return to their lives in their own dimensions. Later, Gwen finds a way to contact Miles from her own dimension.[N 1]

In another dimension, Miguel O'Hara travels to the universe of the 1967 Spider-Man animated series and argues with its Spider-Man.[N 2]