We open on Miles Morales (Shameik Moore), Ordinary High-School Student. Or, at least, so it appears on the surface. In a lot of ways, Miles is a Child of Two Worlds: his father is African-American and his mother is Puerto Rican, and he grew up in NYC; his father, Jefferson Davis (Brian Tyree Henry), is a respected officer of the PDNY, while his Cool Uncle Aaron (Mahershala Ali) is implied to be a little more free-wheeling; he is a gifted graffiti artist, though also technically a vandal; and, despite being from a lower-class borough, has been accepted into the prestigious and upper-class Visions Academy. He could become a lot of things, but his Character Arc will be about figuring out who he wants himself to be. After his first day of school, in which the theme of "Great Expectations" is repeatedly underlined, he runs off with Aaron to an abandoned part of New York's subways to practice his graffiti. Whilst there, Miles is bitten by an unusual spider...
Simultaneously, we open on Spider-Man, the hero of New York. He gives us his Superhero Origin in condensed, telegraphic fashion — though he is played by Chris Pine, his story contains Broad Strokes of events from Sam Raimi's Spider-Man Trilogy starring Tobey Maguire.
The day after being bitten, Miles begins to notice strange things: in addition to a sudden growth spurt, his fingers randomly stick to almost everything he touches, and his senses seem strangely acute. After a great deal of Slap Stick comedy, he remembers the spider bite and and accidentally stumbles upon an old Spider-Man comic book where Peter Parker's troubles mirror his own. He returns to the subway tunnels to look for the spider, only to stumble upon Spider-Man himself fighting against the Green Goblin and the Prowler. The two villains are trying to keep Spider-Man from interfering with the "Super-Collider", a particle accelerator built at the behest of the Kingpin, Wilson Fisk (Liev Schreiber). Miles is drawn into the battle unwillingly, and Spider-Man saves him, with the two, via Spider-Sense, recognizing each other as kindred spirits. Spidey offers to train Miles after handling the Super-Collider. Unfortunately, he is shoved into the nexus created by the Super-Collider, causing a chain reaction that damages the machine and causes dimensional abnormalities throughout NYC.
Miles goes to assist Spider-Man, who is severely injured. Spider-Man gives him a Plot Device that will permanently disable the Super-Collider and stop it from destroying the world. Of course, Miles is untrained and barely has control of his powers; he hides and watches as Fisk stands over the battered and unmasked Spider-Man. Spider-Man warns Fisk that the machine will not bring back his wife and son, who ran from him when they saw him attempt to kill Spidey and died in a car accident shortly after. Fisk, his rage stoked, kills Spider-Man on the spot.
The death of Spider-Man, identified posthumously as Peter Parker, a 26-year-old grad student at Columbia University, is a massive blow to New York. As the city mourns their hero, Miles vows to take up his cause and use his powers to thwart Fisk. Actually being Spider-Man, however, proves to be much harder than he thinks: his outfit is essentially a store-bought Halloween costume (sold to him by Stan Lee in a posthumous cameo), and he continues to struggle with his powers, breaking Peter's Plot Device in the process.
As Miles visits Peter's grave, he encounters the last person he expected to see: Peter Parker!... but Not as You Know Them. Peter B. Parker (Jake Johnson) gives us his Superhero Origin: he is in his late 30s and is getting long in the tooth; he has split acrimoniously from MJ and is out of shape. He is, explicitly, from an Alternate Timeline, and was dragged here recently. When he approaches Miles, he triggers a new power in Miles: the ability to generate a bio-electric current. After a hasty escape from the police, the two converse. Peter simply wants to return home, but Miles convinces him to teach him how to be Spider-Man.
The two go to a laboratory where Fisk's scientists work on the Super-Collider, with the goal being to copy the Collider's schematics, re-create the flash drive that would shut it down, and stop Fisk. While they manage to take a computer containing the schematics, they are found by Fisk's chief scientist, Olivia Octavius (Kathryn Hahn) — AKA Doctor Octopus. As they make their escape and Miles discovers he can also turn invisible, they are assisted by a Spider-Woman: a young woman named Gwen Stacy (Hailee Steinfeld), whom Miles recognizes from school. She, too, hails from another dimension; one in which she was bitten by a radioactive spider instead of Peter Parker, her best friend whose death made her become a loner. She was also pulled into Miles's world by the Collider.
With the computer, the three make their way to the home of May Parker (Lily Tomlin), Peter's aunt. In this continuity, Aunt May became Peter's Secret-Keeper, assisting him by maintaining a secret base under her home. There, Miles and his new friends meet three more Spider-People: Spider-Man Noir (Nicolas Cage), a private detective from the 1930s; Peni Parker (Kimiko Glenn), a young girl with a psychic link to a spider controlling the robot "Sp//dr"; and Spider-Ham (John Mulaney), a cartoon pig. It comes to light that all of the extradimensional Spider-Folx are suffering from cellular degradation due to being in a foreign dimension, and that they will die unless they return to their homes. This is a problem, because someone also needs to ensure the Super-Collider is shut down after the others leave. Miles offers to do it, since he can stay in this dimension safely, but the other Spider-People prove conclusively that he doesn't yet have what it takes to be a hero. Dejected, Miles leaves...
Miles returns to Aaron's home to seek advice, only to discover that Aaron is the Prowler. He returns to May's house to warn the others, only for Doc Ock to arrive with the Prowler, Tombstone, and Scorpion. A brawl breaks out as Miles escapes with the new Plot Device Peni created, only to be cornered by Aaron. As Fisk instructs Aaron to kill the young Spider-Man in his clutches, Miles reveals his identity to him. Aaron relents, only for Fisk to shoot him. Miles escapes with Aaron, who experiences the seminal Death by Origin Story of every Spider-Man, using his dying breath to encourage Miles to follow his own path.
The Spider-People regroup in Miles's dormitory to discuss stopping Fisk. Miles is determined to shut down the Collider so the others can get home, but with his powers still not under control, Peter ties him up and leads the rest to the Collider. Miles's father comes to the dorm and, through his door, apologizes to him for having put so much pressure on him to succeed, resulting in their strained relationship, and reveals that he pushes Miles as hard as he does because he sees so much potential in him. He gives Miles permission to Be Yourself. This unlocks Miles's ability to control his powers; he breaks free from Peter's webs. His next stop is Aunt May's, where he makes his own costume by personalizing one of her nephew's costumes with spray paint and is gifted some hand-made webshooters. NYC may no longer have Peter Parker... But Miles Morales is ready to be the Spider-Man he was born to be.
A brawl breaks out below the streets of Manhattan as Fisk reactivates the Super-Collider, threatening to completely destroy Earth in the vain hope of reuniting with his family. Miles joins the fray, fending off Fisk's enforcers and placing the using the Plot Device to take control of the Collider. Peni, Noir, Ham, and Gwen jump into the beam created by the Collider and return home. Peter B. is the last to go, initially reluctant, but ultimately agreeing to leave the rest in Miles's hands after seeing how his mentee is ready to take on the mantle.
Fisk attempts to kill Miles, their fight leading to Fisk witnessing ghostly visions of his wife and son leaving him in fear upon seeing him almost kill Spider-Man. In the end, however, Miles manages to come out on top, blasting Fisk with electrified webbing and activating the killswitch that destroys the Collider once and for all.
Fisk and his underlings are arrested, the Spider-Men return to their respective worlds, and New York celebrates as a new friendly neighborhood Spider-Man emerges to champion them. Noir has fun with the Rubik's cube he took home with him, Peter B. repairs his relationship with Mary-Jane Watson, Peni repairs SP//dr after it was damaged fighting Scorpion, Gwen discovers a way to contact Miles across dimensions, and — in The Stinger — Spider-Man 2099, Miguel O'Hara (Oscar Isaac), attempts some multiverse-traveling of his own...
