In *Pokémon the Movie: Secrets of the Jungle*, Meowth operates as a member of Team Rocket alongside Jessie and James. Covertly tracking Ash Ketchum and Dr. Zed's Biotope Company research team into the Forest of Okoya, Team Rocket infiltrates the team to uncover Dr. Zed's activities and intentions. During the climax, Meowth and his teammates inadvertently assist Ash and Koko by wrestling with a wild Cramorant, creating a crucial distraction that enables Ash and Koko to escape capture from one of Dr. Zed's trucks. Team Rocket subsequently leaks evidence of Dr. Zed's crimes, resulting in his arrest by Officer Jenny.

Meowth's background across the broader anime series reveals he was abandoned as a kitten in Hollywood, struggling to survive on the streets. He joined a gang of Meowth led by a Persian, surviving through theft. Infatuation with a female Meowth named Meowzie led him to dedicate himself to learning human speech and walking upright to impress her, sacrificing his ability to learn moves like Pay Day. After achieving this, Meowzie rejected him again, calling him a "freak," prompting him to join Team Rocket.

Within Team Rocket, Meowth serves as the trio's mascot, strategist, and primary inventor of their gadgets and vehicles. His unique ability to speak human language and translate Pokémon speech is central to their operations, though it limits his combat effectiveness. He harbors a strong dislike for Persian, especially Giovanni's Persian, which replaced him as Giovanni's favored Pokémon. Despite frequent internal conflicts with Jessie and James, Meowth demonstrates unwavering loyalty to them, repeatedly choosing to stay with Team Rocket over opportunities for fame or legitimate careers. He has occasionally displayed philosophical depth, empathy for abandoned Pokémon, and culinary talent, particularly in noodle-making.