Rolston played PFC M. Drake in Aliens (1986), Hans in Lethal Weapon 2 (1989), Stef in RoboCop 2 (1990), Bogs Diamond in The Shawshank Redemption (1994), J. Scar in Eraser (1996), Chief Dennis Wilson in Daylight (1996), Wayne Bryce in Hard Rain (1998) and Special Agent Warren Russ in Rush Hour (1998).
Rolston acted in Martin Scorsese's 2006 film The Departed and the television horror film Backwoods. Many of Rolston's screen roles are villains due to his well-known icy stare. He also co-starred in 2008's Saw V and 2009's Saw VI. In 1994, he portrayed convicted killer "Karl Mueller" in the Babylon 5 episode "The Quality of Mercy", as well as "Richard Odin", leader of a vegetarian cult in an episode of The X-Files titled "Red Museum". He was also originally considered to voice the supervillain Firefly in Batman: The Animated Series in 1992, although the character was deemed unsuitable for the series and ultimately dropped.
Rolston later voiced Firefly in The New Batman Adventures and Justice League. In 2004, Rolston would guest star in two episodes of the critically acclaimed 24. He appeared in a minor role in The CW series Supernatural during the fourth season as the demon Alastair. He also appeared as Sheriff Hall in the Criminal Minds episode, "Blood Hungry".

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