The film starts with Peter Parker (Chris Pine) introducing himself as we know him, the friendly neighborhood Spider-Man. By now, everybody knows how big he is, what with saving New York constantly, getting his own comics, cereal, and even a Christmas album. He does have some things he's not proud of (the emo dance, for one), but he takes his duties as Spidey proudly, as he is the one and only.
We meet Brooklyn teen Miles Morales (Shameik Moore) as he is getting ready to start attending a private school. He lives with his father Jefferson (Brian Tyree Henry) and mother Rio (Luna Lauren Velez). Miles goes around his neighborhood greeting his friends and tagging street signs with stickers he made. Jefferson, a cop, catches Miles and escorts him to school in his cruiser. As they ride to the school, they see a news report on Spider-Man, whom Jeff is not a fan of. Once they arrive, Jeff tells Miles he loves him, but Miles fails to say it back. Jeff then uses his radio to force Miles in front of all the other students to say "I love you" back, embarrassing him.
Miles gets into his schoolwork as he tries to adjust to this new environment. During one of his classes, he meets Gwen Stacy (Hailee Steinfeld), who doesn't immediately tell him who she is. Later, Miles sneaks out of his dorm to visit his uncle Aaron (Mahershala Ali), who is Jefferson's brother and a sort of black sheep due to his criminal activities. Miles tells him about Gwen, and Aaron tells him to do a shoulder touch to try and charm her. The two then go to the tunnels near the subway so that they can do some graffiti, since Aaron is fond of Miles's artwork. As Miles spray-paints the walls, a radioactive glitching spider crawls up his leg and bites his hand after Miles takes a picture of his work, but he only lightly taps the spider off his hand before leaving with Aaron.
The next day, Miles finds himself feeling differently. He hears a voice in his head (which is accompanied by comics-style text boxes), his clothes barely fit, and he is sweating profusely. He runs into Gwen, who tries to make up a fake name when they properly introduce themselves. Miles tries to do the shoulder touch, but he only gets his hand stuck on Gwen's shoulder, and then her hair, leading them to have to go to the nurse for her to cut her hair off. When Miles tries going back to his room, he is found by a security guard who calls him out for leaving his dorm. Miles runs and hides in the man's office, getting everything stuck to him as he keeps freaking out. He climbs out the window and finds himself walking on the walls before running into the streets, amazed by his newfound powers and abilities.
Miles later goes to the tunnel where the spider bit him. As he examines it, it starts glitching again. Not long after, Miles hides as his spider sense detects danger. Spider-Man enters as he's being pursued by the Green Goblin (Jorma Taccone). The fight takes them beneath Fisk Industries where Wilson Fisk/Kingpin (Liev Schreiber) is attempting to start up a Super Collider. In the middle of Spidey fighting Goblin, he takes the time to get Miles out of harm's way. Spidey realizes Miles is just like him, just as the machine is turned on. Outside in the city, certain structures start to get weirdly morphed into other shapes. A blast occurs in the tunnel. Spidey is badly injured, and Miles tries to help him, but Spidey tells him to hide before giving him a drive to shut down the Collider. Kingpin, Goblin, and another villain, The Prowler, gather around Spidey and remove his mask. He begs Kingpin not to restart the Collider, even telling him to think about his family, but this angers Kingpin and he kills Spider-Man by slamming his fists down onto him, which Miles watches in horror. He runs back home where his parents find him, and he runs to hug Jefferson.
The news breaks out that Spider-Man is dead, and that he was Peter Parker. New Yorkers everywhere are devastated. Miles buys a costume (from Stan Lee, no less) before attending a memorial service for Peter, with many other fans attending dressed as the wallcrawler. Mary Jane (Zoe Kravitz) delivers a eulogy for her husband while Aunt May (Lily Tomlin) stands solemnly in the back.
Miles is inspired by MJ's words to take up the mantle as Spider-Man. He wants to test out his powers, but he isn't quite sure of how to get them to work. He later pays a visit to Peter's grave, just as he is spotted by another man...Peter B. Parker (Jake Johnson). In his own words, this Peter tells us that in his universe, he's been Spider-Man for years and is now an adult, but he's lost Aunt May and he was married to Mary Jane but is now divorced due to him not being able to work out his issues as Spidey, as well as him not wanting kids when she did. He became depressed and gained weight, and then the Collider turned on, which pulled him into this dimension. Now after finding Miles, he gets knocked unconscious, leading Miles to try and swing away with him as the police go after them, only to end up crashing on the streets as people walk past them.
Miles brings Peter somewhere for safety. He questions Peter as to how it's possible that he's there alive, when he correctly guesses the alternate dimension theory. Miles takes out the drive that the Peter of his universe gave him (which other Peter calls a "goober"), but it's broken. Peter frees himself and takes the broken goober to try and find a new one so that he can get back home, as being in this dimension causes him to glitch and be unstable. However, before Peter can head off on his own, Miles guilts him into letting him join so that they can make things right together.
Miles and Peter, dressed in their costumes, go to Alchemax Labs where the data on the Collider is being kept. As they try to find a way to sneak in, Kingpin and his henchman Tombstone (Marvin "Krondon" Jones III) and his top scientist (Kathryn Hahn). Kingpin's motive for operating the Collider is to be reunited with his wife Vanessa (Lake Bell) and son Richard. Years earlier, they watched as he tried to kill Spider-Man, and they fled from him, only to be tragically hit by a truck.
Miles and Peter manage to sneak into the lab and find the room with the computer. Miles starts freaking out again as he can't unstick himself from the ceiling, just as Kingpin and his scientist are outside. Miles then also finds out he can turn invisible while he's scared. The scientist then enters the room, forcing Peter to try and charm her. She is impressed to find Spider-Man alive, but only so she can kill him herself. She then reveals her name to be Dr. Olivia Octavius, aka DOC OCK. She reveals her mechanical tentacles as she attacks Peter, but Miles grabs the computer so that they can go. They are chased by scientists out of the lab and into the woods. The guys swing through the trees as the villains catch up, but Doc Ock gets webbed up by a third spider-person...GWEN. She tells Miles and Peter how she too has come from another dimension where she was bitten by a spider. There, she saved her father's life but couldn't save Peter. The three of them then head out of the woods to get away. Doc Ock later goes back to Kingpin, who is highly displeased to find there are two more Spider-Men around.
Miles, Peter, and Gwen to go Aunt May's home, where she is able to figure out that the Peter she sees before her is from another dimension. She takes them to her Peter's old secret hideout, which is full of different suits, gadgets, and vehicles. There, the three meet Spider-Man Noir (Nicolas Cage), a black-and-white old-gangster-talking hero; Peni Parker (Kimiko Glenn) and her robot SP//dr, which is powered by a radioactive spider; and Peter Porker, aka Spider-Ham (John Mulaney), who was actually a spider bitten by a radioactive pig. All of them were pulled from their own dimensions and into Miles's world. They each plan to stay behind and shut down the Collider with a new goober so that the rest can get home, but Miles says it has to be him since this is his dimension. When Peter tries to back him up by stating the cool powers that Miles has, he is unable to turn them on and prove to the others that he is capable of helping. Miles turns invisible and he dejectedly leaves the cave.
Miles goes to Aaron's home for help, just as Jefferson and Rio are contacting Aaron since they haven't heard from Miles in a while. Miles finds Aaron's apartment empty, but then encounters Prowler inside, prompting him to go invisible again. Prowler speaks to Kingpin and removes his mask, revealing himself to be Aaron. Miles is horrified. He tries to get out of the apartment but is chased by Aaron throughout the city until he manages to evade him.
Back at Aunt May's house, Miles reunites with the other Spider-People to tell them that his uncle is working for Kingpin. Unfortunately, Miles has led Prowler there, along with Doc Ock, Goblin, Tombstone, and Scorpion (Joaquin Cosio). The villains attack, and the Spider-People spring into action. Even Aunt May gets in on it by defending her home. Prowler goes after Miles and chases him to the rooftop. Kingpin orders Prowler to finish Miles off, until Miles takes off his mask to reveal himself to his uncle. Aaron is mortified that he almost killed his nephew. As he backs down, Kingpin shoots Aaron in the back and then goes for Miles, but he swings out of there with his uncle. He takes Aaron to an alley where he is dying. Miles blames himself for what happened, but Aaron encourages him to keep pushing forward. Jefferson finds Miles over Aaron’s body, sending Miles fleeing. Jeff then sees his brother and breaks down.
Miles returns to his dorm where the other Spider-People meet up with him. They cause his roommate to pass out from seeing them crawl up the wall. Peter webs Miles up to his chair and takes the goober to go stop the Collider, telling Miles it’s for his safety. After they leave, Jeff comes up to Miles’s dorm outside, but he can’t respond thanks to the web. Jeff tells him about Aaron and only wishes for Miles to be okay. Miles then musters up the strength to bring out his power to free himself.
Miles goes back to Aunt May’s and gets the original Spider-Man suit, which he spray paints with dark colors. He then tests his powers more confidently as he swings around the city.
The other Spider-People find Kingpin’s gala where they are able to sneak in because the staff are wearing Spidey masks. Peter sees MJ and tried to express his guilt toward leaving her, even though she doesn’t know it’s him or what he’s talking about. They proceed down to where the Collider is, but Kingpin’s henchmen find them and proceed to attack. Miles swings in and joins his comrades as they fight back. To make things worse, the Collider is activated, causing another earthquake across the city as dimensions start warping together.
Spider-Man Noir takes on Tombstone while Peni and SP//dr fight Goblin, and Spider-Ham beats up Scorpion with a cartoon mallet. Doc Ock goes after Gwen and Peter while Miles tries to shut the Collider down. The henchmen are taken out, and Doc Ock is plowed by an interdimensional truck. Unfortunately, SP//dr is heavily damaged, leaving Peni devastated as Noir and Spider-Ham comfort her. She takes the spider back as they prepare to jump back home. They say their farewells, and Peni goes first, followed by Noir and Spider-Ham. Gwen affirms her friendship with Miles before going home. Peter tried to stay back and help Peter, but Miles chooses to send Peter back so that he can fix what he has to do in his world. Miles then goes after the Collider, but Kingpin starts hitting back hard. He then starts to see a new Vanessa and Richard as their dimensions start crossing over. Just as Kingpin seems to overpower Miles, he sees Jefferson as he enters the area. Miles gets himself up and uses his power to blast Kingpin away and then send him webbed up toward the button to shut down the Collider for good.
Outside, Miles calls Jeff to let him know he’s okay. He then approaches him as Spider-Man and hugs him, letting him know he’s doing a good job, but not letting his dad know who he really is. Jeff then finds Kingpin webbed up and prepped for arrest.
Miles now assumes his regular school duties while also taking on his role as the new Spider-Man, earning a number of new fans across the city. Meanwhile in Peter’s dimension, he heads off to patch things up with MJ. As Miles settles in his room for a nap, a dimensional portal opens and he hears Gwen’s voice calling to him.
There is a dedication for Stan Lee and Steve Ditko.
After Credits: Miguel O’Hara/Spider-Man 2099 (Oscar Isaac) learns about the other Spider-People from his assistant Lyla (Greta Lee). He travels to Earth 67 where he ends up in a weird pointing argument with the Spider-Man from the 60’s cartoon.
*CUT TO THE CHASE*
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Brooklyn teen Miles Morales is given powers after a radioactive spider bites him. He comes across a Super Collider established by Wilson Fisk/Kingpin, which he is using as a means to find another dimension where his wife and child are alive. After a fight with the Green Goblin, Fisk murders Peter Parker, leaving all of New York mourning Spider-Man.
The Collider opens up multiple dimensions that bring other Spider-People to Miles’s universe. He meets an alternate Peter Parker whose life has gone downhill, including a divorce from Mary Jane. They team up with Gwen Stacy/Spider-Woman, Spider-Man Noir, Peni Parker, and Spider-Ham. They fight back against Kingpin’s henchmen, which include Goblin, Doc Ock, Scorpion, and Prowler, who is secretly Miles’s uncle Aaron Davis. Kingpin kills Aaron after he refuses to kill Miles. The Spider-People decide to stop Kingpin themselves because Miles is inexperienced. However, he musters up the strength and courage to fight back himself.
The Spider-People attempt to stop the Collider at a gala, and Miles heads in to join them. They fight off the henchmen as the Collider turns on and the dimensions are open. The Spider-People head home while Miles stays to fight Kingpin and shut down the Collider. Kingpin is arrested.
Miles becomes the new Spider-Man of his universe and may have found a way to keep in touch with Gwen through dimensions. Meanwhile, Peter is going to fix things with Mary Jane.
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