A large robotic craft arrives searching for Susan Strong. However, when it reaches the Bubblegum Kingdom, Jake destroys it with his fist. Princess Bubblegum examines the wreckage and discovers its location of origin leading Finn wanting to discover its creators. Before leaving, Finn tells Fern to stay and look after Ooo for him. Princess Bubblegum, Marceline and Fern see Finn, Jake and Susan off on their voyage.
Finn, Jake, and Susan encounter a sea dragon named Whipple (voiced by Josh Fadem) who turns out to be rather annoying. BMO, who stowed away on their boat, angrily tells Whipple off. BMO summons a storm and destroys their boat forcing Jake to fill in. Jake begins to hallucinate his parents after a species of jellyfish latch onto him, but Finn and Susan are able to fight them. After Jake complains about wanting to return home, Finn reveals how important this trip is to him. Whipple overhears Finn's lament and uses his powers to blow the group over the dangerous waters.
After an encounter with a colossus, Finn wakes up on an island where the weather drastically fluctuates. He encounters an old lady named Alva (voiced by Helena Mattsson) who does not speak English. Alva invites Finn to her home and shows her home movies of other humans who have presumably died. Later Finn, Alva and her pet bear encounter Jake who does not know the whereabouts of BMO and Susan. On the moon, BMO is being attended to by another robot and wishes that Finn, Jake and Susan could join her.
Finn and Jake head to a futuristic island where all of society has hooked themselves up to a virtual reality simulator. BMO is revealed to actually be in that simulation becoming a heroic leader along with his sidekick Vinny (voiced by Reggie Watts). Jake decides to go and destroy the generator powering the VR after BMO refuses to leave. Feeling bad for BMO, as well as the emaciated humans, Finn asks Jake to fix the generator, but BMO fixes it himself. BMO returns to Finn and Jake and they take a pod to the next island.
Finn, Jake and BMO find Susan who begins to have glimpses of her past. Susan, whose real name is Kara, is a seeker in training whose job is to bring those who try to flee from paradise. Kara is friends with Frieda (voiced by Jasika Nicole) who expresses the desire to flee which causes Kara some discomfort. She approaches Dr. Gross (voiced by Lennon Parham) asking if they can live off the island. When Dr. Gross convinces her that the outside is dangerous, they stop Frieda from leaving, dragging her away crying. Back in the present, Susan tells Finn her real name.
Kara decides to take Finn to Founders Island so that he can be reunited with his mother, Minerva Campbell (voiced by Sharon Horgan). Flashbacks detail how Minerva, a nurse, met Finn's father Martin Mertins (voiced by Stephen Root) when he was hospitalized after it was mistakenly believed he was attempting to leave the island with a group of escapees. Martin and Minerva fall in love and have Finn. When one of the attempted escapees, an elderly widow (voiced by Laraine Newman), seeks revenge on Martin, he flees on a boat with Finn. When the colossus attacks their craft, the pair are separated, leaving Finn to drift away. The widow is arrested and Minerva is heartbroken over Martin and Finn's disappearance.
The group make it to Founders Island where humans have been living in relative peace. While Kara is distracted by Frieda, Finn and Jake discover that the island is full of Minerva look-alike robots called "helpers". They are brought to the real Minerva—a digitized consciousness—when Finn is identified as her son. Minerva reveals that she had Dr. Gross send Kara to retrieve Finn, but years had passed and Dr. Gross accidentally released a deadly virus that was killing humans. Minerva had her essence uploaded into a computer, and then created the helpers to prolong the human race. But now that Finn is here with her, she expresses her desire that he stay permanently.
While Susan makes amends with Frieda, Finn tries to convince Minerva that life off the island isn't bad, but Minerva thinks it's dangerous. Finn then tries to convince the humans to leave and they all rally alongside him. Minerva tries to upload the consciousnesses of all the islands' inhabitants, so Finn shares with her his memories of helping people, causing her to back down. The humans all change their minds about leaving, except for Frieda. With Minerva's help, they defeat the colossus and Susan and Frieda leave for parts unknown. Finn has one final talk with Minerva through the VR headset before returning to Ooo with Jake and BMO.