Meowth operates as a core Team Rocket member alongside Jessie and James. This feline Pokémon uniquely taught himself human speech and upright walking, aiming to impress a female Meowth named Meowzie during his Hollywood street days. After this rejection branded him a "freak," he recalled "rocket" as the first human word he understood and joined the organization.

Within the team, Meowth acts as the primary strategist and translator, frequently constructing devices and interpreting Pokémon speech. His focus on human-like abilities cost him combat prowess, leaving him unable to master his species' signature move, Pay Day. Despite constant squabbles, he remains loyal to Jessie and James. He harbors deep jealousy toward Persian, especially Giovanni's Persian, which supplanted him as the "top cat."

In *Pokémon the Movie: Diancie and the Cocoon of Destruction*, Meowth participates in Team Rocket's plot to exploit the Mythical Pokémon Diancie for her diamond-creating power. Witnessing Diancie's formal address, the trio kidnaps her and coerces diamond production inside a clock tower. The resulting overflow of diamonds jams the clock's mechanism, aligning with Meowth's species-typical attraction to shiny objects.

His personality mixes cunning with occasional philosophical depth. He displays greed and pride, yet shows empathy for abandoned Pokémon, echoing his own harsh past. While often considering himself the trio's leader, his schemes, including the diamond heist, consistently end in failure. He consciously remains unevolved, partly fueled by his disdain for Persian.