Miles Morales' name and picture appears in the episode "I Am Spider-Man" on a list of understudies for the part of Spider-Man in Phil Coulson's high school play. He is the second to last choice, while Peter Parker is the last choice. In May 2014, the Sunday badge for the 2014 New York Comic Con was revealed, featuring the third season title Ultimate Spider-Man: Web-Warriors, and showing various incarnations of Spider-Man, including one wearing Miles Morales' costume. Web Warriors is a third season storyline in which Peter Parker travels through various parallel universes, and encounters those dimensions' versions of Spider-Man, including Miles Morales.
Miles eventually appears in Parts 3 and 4 of the Spider-Verse arc, which involves him teaming up with Spider-Man and other incarnations of Spiders to defeat a dimension-hopping Green Goblin. In the episode "Miles from Home", Miles had a brief fight with his Green Goblin while getting his mother Rio (who in this reality knows Miles is Spider-Man) a birthday cake. However, Baron Mordo helps Doctor Octopus bring the Green Goblin of Miles' universe to combat his Spider-Man, and Peter brings Miles to assist him. Their fight results in Miles getting stuck in Peter's reality. Doctor Strange opened a temporal window so that Miles could let his mother know that he's all right and he will find a way back to her. Spider-Man then took Miles to the Triskelion where he met Agent Venom, Iron Spider, and Scarlet Spider. It was decided that he would live there for the time being until they would find a way to bring Miles back to his own dimension. In the episode "Iron Vulture", Spider-Man, Miles Morales, and Agent Venom defeated Batroc the Leaper. Later on, Miles meets Harry Osborn and Norman Osborn before they are attacked by Vulture and Doctor Octopus. Due to a naming by Doctor Octopus, Miles Morales uses the alias of Kid Arachnid as he helps Spider-Man and Norman Osborn in his Iron Patriot armor defeat Doctor Octopus and Vulture.
In Ultimate Spider-Man, Miles' decision to become his dimension's Spider-Man after the death of his Peter Parker was lifted from the comics. The only difference between this version and comic Miles is that his mother Rio knows he's Spider-Man and supports his actions, whereas the canon version didn't know Miles was Spider-Man until her death, but she was resurrected and her knowledge was retconned (though Miles' father, Jefferson Davis, knew).
This version's Jefferson Davis is hinted to be deceased when Rio referred to him in "Miles from Home". It is further implied in "Return to Spider-Verse Part 4", when Rio claims that Miles is the only family she has left.
Miles' first actor, Donald Glover, was one of the original inspirations for Miles' character from his unsuccessful attempt to be cast as the lead in the 2012 Amazing Spider-Man reboot.