Gilliam started his career as an animator and strip cartoonist. One of his early photographic strips for Help! featured future Python cast-member John Cleese. When Help! folded, Gilliam went to Europe, jokingly announcing in the very last issue that he was "being transferred to the European branch" of the magazine, which of course did not exist. Moving to England, he animated sequences for the children's series Do Not Adjust Your Set, which also featured Eric Idle, Terry Jones, and Michael Palin.
Gilliam was a part of Monty Python's Flying Circus from its outset, at first credited as an animator (his name was listed separately after the other five in the closing credits), later as a full member. His cartoons linked the show's sketches together, and defined the group's visual language in other media (such as LP and book covers, and the title sequences of their films). Gilliam's animations mix his own art, characterized by soft gradients and odd, bulbous shapes, with backgrounds and moving cutouts from antique photographs, mostly from the Victorian era.
Besides doing the animations, he also appeared in several sketches, though he rarely had any main roles and did considerably less acting in the sketches. He did however have some notable sketch roles such as Cardinal Fang of the Spanish Inquisition, "I Want More Beans!" (from "Most Awful Family in Britain 1974", Episode 45) and the Screaming Queen in a cape and mask singing "Ding dong merrily on high." More frequently, he played parts that no one else wanted to play (generally because they required a lot of make-up or uncomfortable costumes, such as a recurring knight in armour who would end sketches by walking on and hitting one of the other characters over the head with a plucked chicken) and took a number of small roles in the films, including Patsy in Monty Python and the Holy Grail (which he co-directed with Terry Jones, where Gilliam was responsible for photography, while Jones would guide the actors' performances) and the jailer in Monty Python's Life of Brian.