[4][5] Directed by Bob Persichetti, Peter Ramsey, and Rodney Rothman from a screenplay by Phil Lord and Rothman, it stars Shameik Moore as Morales, alongside the voices of Jake Johnson, Hailee Steinfeld, Mahershala Ali, Brian Tyree Henry, Lily Tomlin, Luna Lauren Vélez, John Mulaney, Kimiko Glenn, Nicolas Cage, and Liev Schreiber.

Lord and Miller wanted the film to have a unique style, combining computer animation with hand-drawn comic techniques inspired by the work of Miles Morales co-creator Sara Pichelli.

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.

Returning to the station where he got bit, he discovers a collider built by Kingpin, who hopes to access parallel universes to abduct alternate versions of his late wife Vanessa and son Richard.

[25][26][27] A young Matt Murdock from Gwen's dimension appears in an "Easter egg" cameo during Morales' final train fight scene as an alternate universe adopted son of Kingpin.

This scene, a reference to an unsuccessful Twitter campaign suggesting Glover be cast in the lead role of The Amazing Spider-Man (2012),[31] was cited by Miles Morales' creator, Brian Michael Bendis, as influencing the design and portrayal of the character.

[44] In February 2017, Alex Hirsch was named as a story contributor and Christina Steinberg replaced Tolmach as a producer; she previously collaborated with Ramsey on Rise of the Guardians (2012) while at DreamWorks Animation.

[50] Rothman was initially added as a writer on the script, fulfilling duties Lord was unable to do due to commitments to Solo: A Star Wars Story and other projects, and as production progressed he wished to be a director.

As he was the only co-writer Lord would "fully endorse", and since it was typical that writers would be involved in editorial processes with directors, Rothman wanted to fulfill a role "beyond this".

[52] One year prior to its release, Lord and Rothman opted to rewrite the story as they had to "figure out how to reshape sequences we had already boarded and animated and fold them in with new stuff".

[52] At one point the writers wished to include a post-credits scene with cameos by all three live-action Spider-Man actors, Tobey Maguire, Andrew Garfield, and Tom Holland, but this was canceled as Sony felt such a moment at the time would cause confusion and be too risky.

[62] In June 2018, Sony confirmed further casting, including Schreiber playing Kingpin, Hailee Steinfeld as Spider-Gwen, Luna Lauren Vélez as Morales's mother Rio, and Lily Tomlin as Parker's Aunt May.

[67] Artists on the soundtrack include Jaden Smith, Nicki Minaj, Lil Wayne, Post Malone, Ty Dolla Sign, Juice Wrld, Swae Lee, Ski Mask the Slump God, Vince Staples, Thutmose, and the late XXXTentacion, who was marketed as a special guest on the Lil Wayne and Ty Dolla Sign song "Scared of the Dark".

[77] Justin K. Thompson served as production designer after having done so on the Cloudy with a Chance of Meatballs films for Lord, Miller, and Sony Pictures Animation.

[85] The directors all felt that the film would be one of the few that audiences actually "need" to watch in 3D, due to the immersive nature of the animated world created, and the way that the hand-drawn animation elements designed specifically for the film create a unique experience; Persichetti described the experience as a combination of the effects of an old-fashioned hand-drawn multiplane camera and a modern virtual reality environment.

[88] The official trailer for the film was released online at the start of June 2018, and was praised by Chaim Gartenberg of The Verge for its "absolutely gorgeous" art style, also highlighting Miles and Gwen's appearances.

[42] For Cartoon Brew, Amid Amidi praised the trailer for focusing on drama rather than action, and for seemingly targeting "a slightly hipper, more urban, and teen-oriented crowd."

[89] Dani Di Placido of Forbes praised the trailer for inspiring interest in the Spider-Man property after several different incarnations of the character had appeared in films.

[51][92] Lord and Miller explained that they chose not to show clips from throughout the film because they would lack context for the audience, so instead aired an extended sequence for the presentation, even though it had some unfinished animation and music.

[41][43][49] Sony premiered the film at the Regency Village Theater in Los Angeles on December 1, 2018, and included tributes to Stan Lee and Steve Ditko.

[110] On March 1–3, the weekend following its Best Animated Feature win at the Academy Awards, the film was added to 1,661 theaters (for a total of 2,104) and made $2.1 million, marking a 138% increase from the week before.

The website's critical consensus reads, "Spider-Man: Into the Spider-Verse matches bold storytelling with striking animation for a purely enjoyable adventure with heart, humor, and plenty of superhero action".

[107] David Ehrlich of IndieWire gave the film a "B+" and called it "hilarious and ultimately even poignant", writing, "An eye-popping and irreverent animated experience from the marvelous comic minds who brought you 21 Jump Street...

"[118] Todd McCarthy of The Hollywood Reporter wrote, "the freshest and most stimulating aspect of the film is the visual style, which unites the expected Marvel mix of 'universes' (it used to be assumed there was only one universe in creation) with animation that looks both computer-driven and hand-drawn, boasts futuristic as well as funky urban elements, moves the 'camera' a lot and brings together a melting pot of mostly amusing new characters.

"[121] David Sims of The Atlantic said that the film "somehow, through sheer creative gumption, does something new in the superhero genre", particularly praising the use of comic book's "visual language" as well as the characters' dynamic, and felt that the "anarchic fingerprints" of producers Lord and Miller were "all over the movie".

"[125] Chris Pratt, who worked with Lord and Miller on The Lego Movie films, described it as an "emotionally moving, cutting edge, progressive, diverse, funny, meta, action-packed, silly, visually stunning masterpiece!

"[133] Many other filmmakers including Edgar Wright, Guillermo del Toro, Yance Ford, and RaMell Ross have listed the film as one of their favorites of 2018.

[135][138][139] Directors Adil El Arbi and Bilall Fallah said Spider-Verse inspired them to create the hand-drawn style of visual effects for the live-action MCU series Ms. Marvel (2022).

[161] In 2018, Sony announced a spin-off animated film based on the Spider-Women comics, focusing on three generations of female Spider-related characters,[162] including Spider-Gwen, Jessica Drew / Spider-Woman, and Cindy Moon / Silk.

[164] John Mulaney expressed interest in a potential spin-off film starring Spider-Ham, suggesting its plot as a "Watergate-like story" along the lines of The Post or All the President's Men while focusing on his character's career as a reporter.