Hailed by the British film researchers of "Film Dope" as "the loser's loser", Miller earned his cultish credentials with an indelible starring performance in "A Bucket of Blood" (1959), Corman's spoof of the beatnik art scene. Miller's Walter Paisley was a coffee shop busboy turned celebrated sculptor-cum-serial killer who wins acclaim by presenting the corpses of his victims encased in clay. VARIETY accurately observed that "Dick Miller's ability to sustain a sense of poignancy while acting conceited and committing atrocities is responsible for a large part of the picture's appeal." His other roles for Corman include playing an unfortunate vacuum cleaner salesman in "Not of This Earth" (1956), a college student accused of impregnating a co-ed in "Sorority Girl" (1957), and an unlikely rocket scientist in "War of the Satellites" (1958).

Miller became a good luck charm and directorial private joke after Corman left AIP and formed New World Pictures in 1970. There the actor began associating with some future major players including Martin Scorsese, Jonathan Demme, Joe Dante and Jonathan Kaplan. Miller was a regular in a number of Kaplan-directed potboilers including "The Student Teachers" (1973) as a unsympathetic gym teacher and the Isaac Hayes Blaxploitation vehicle "Truck Turner" (1974). He was also featured in a more upscale biopic of female racecar driver Shirley Muldowney, in Kaplan's "Heart Like a Wheel" (1983). By the end of 1994, Miller had appeared in eight of Kaplan's films and ten of Dante's.

Miller continued working regularly throughout the 80s and into the 90s in both film and TV. He appeared in James Cameron's "The Terminator" (1984) as the pawn shop clerk who provides Schwarzenegger with weapons, and popped up in Scorsese's "After Hours" (1985) as a waiter in an all-night restaurant. Miller's other feature credits include Dante's "Matinee", the animated "Batman: Mask of the Phantasm" (both 1993), Quentin Tarantino's "Pulp Fiction" (1994), and "Tales From the Crypt Presents Demon Knight" (1995).