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O primeiro papel de Larroquette não foi creditado, como um soldado do exército em Follow Me, Boys! (1966). Ele também fez um papel não creditado como narrador na versão original de O Massacre da Serra Elétrica (1974). Seu papel mais memorável em séries "sérias" foi na série de nome Baa Baa Black Sheep, dos anos 70, onde ele interpretava um fuzileiro naval americano chamado Luke Witkowski.
Larroquette abriu suas portas na TV na novela Doctors' Hospital, e talvez seja bem lembrado (principalmente nos EUA) pelo personagem Dan Fielding em Night Court, papel pelo qual o ator venceu o Emmy Award em 1985, 1986, 1987, e 1988. Em 1989, ele pediu para não ser indicado ao Emmy. Suas 4 vitórias consecutivas foram, à época, um recorde. Night Court era transmitido no canal NBC de 1984 até 1992. Somente Larroquette, Harry Anderson, e Richard Moll (como Bull Shannon) apareceram em todos os episódios da série.
Larroquette mais tarde estrelou o The John Larroquette Show no papel de John Hemmingway. O programa agradou aos críticos e muitos seguidores cult. Estrelou em filmes como Second Sight, com Bronson Pinchot, and Madhouse, com Kirstie Alley. Outros filmes em que Larroquette teve papéis significantes incluem: Blind Date, Stripes, Meatballs Part II, Summer Rental, Star Trek III: The Search for Spock, JFK e Riquinho.
Em 2003, Larroquette narrou o remake de O Massacre da Serra Elétrica, desta vez devidamente creditado.
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