The Director of four feature films, Miller is probably best known for directing the seasonal film Jack Frost, starring Michael Keaton. Miller also directed the Mr. Show spin-off movie Run Ronnie Run! which opened the Sundance Film Festival in 2002 and CineVegas' closing night film that same year. Among other features and movie-of-the-week productions, Miller also directed Dumb and Dumberer: When Harry Met Lloyd, a moderate commercial success in first release. The film was poorly received by critics and on Rotten Tomatoes, but it went on to earn upwards of $80 million in international box office. Miller also directed The Announcement, an independent feature, made in the UK and distributed by the BBC1, that starred Mark Addy among others.

Miller has produced and directed short- and long-form programming for all of the major networks (ABC, NBC, CBS, Fox) and cable outlets such as MTV, Comedy Central, Bravo, TBS, Disney XD, and many others including the BBC. Some notable projects from Miller's past include Mr. Show and Tenacious D for HBO, on which Miller served as both executive Producer and Director. In 2003, Miller created Viva La Bam along with Celebrity skater Bam Margera for MTV; by 2005 it was the most watched cable show for teens aged 12–18. Miller's first industry job was as an intern on the show Fridays, working under the tutelage of comics such as Rich Hall, Larry David and Andy Kaufman. Miller directed all episodes in the first two seasons of the Emmy-nominated Tracey Ullman's State of the Union for Showtime, and regularly directs episodes of NBC's Parks and Recreation and The Office. Miller is executive Producer and one of the Directors for both seasons of the acclaimed shows Flight of the Conchords as well as HBO's Bored to Death. When directing an episode, Miller often operates Steadicam. Most recently Miller directed/executive produced (with creator Mitch Hurwitz) the fourth season of Arrested Development for Netflix. Other recent credits include EP/Director/Creator of FX's BrandX with Russell Brand as well as Parks and Recreation, The Office, and New Girl.

Miller has also produced and directed eight opening films for the Academy Awards Oscar telecast, including those featuring Billy Crystal, Jon Stewart, James Franco and Anne Hathaway. He is the creator of this "short film opening award show format" that ultimately began with the MTV Movie Awards. His films have served as the opening for twenty awards shows. Miller is one of the creators of the short-form genre of films that have become Common in award show openings. Having produced and directed many MTV Movie Awards opens, including the two most recent shows hosted by Conan O'Brien and Rebel Wilson respectively. Miller produced and directed all of the short films that have opened the Oscar telecast. The 84th annual show featured Tom Cruise and George Clooney and again featured Billy Crystal (embedded within the footage of other films). In 2006, Jon Stewart used Miller to construct his Oscar open which featured Clooney, Chris Rock, Halle Berry, Steve Martin and David Letterman. Miller also directed the opening film for the 83rd Academy Awards parodying Inception, featuring hosts Franco and Hathaway embedded in Best Picture nominees and cameo appearances by Alec Baldwin and Morgan Freeman. Miller also crafted the opening film for Bette Midler's Las Vegas stage show, The Showgirl Must Go On as well as has directed well a huge array of other short films for various Sketch programs and live presentations and film festivals.

Most recently, Miller directed and produced all ten episodes for Hulu's biggest original project to date, Deadbeat, which was shot in New York City and features performances by Tyler Labine, Cat Deeley, Brandon T. Jackson and Lucy DeVito. Deadbeat premiered on April 9, 2014 to positive reviews and was #1 site wide the day it dropped on Hulu. Currently, Miller has several projects in development through his production shingle Dakota Pictures. Previously, Miller acted as Producer and Director of the Netflix reboot of Arrested Development, along with the show's creator Mitch Hurwitz. Prior to Arrested, he also executive produced and directed HBO’s George Lopez: It's Not Me, It's You, a live comedy concert and one of HBO's most watched events of 2012. Miller has produced and/or directed specials for a variety of many other comedians including Robin Williams, Martin Short, Katt Williams, Jim Gaffigan, Brian Regan, Dave Chappelle, David Cross, Kathleen Madigan, Jeff Garlin, and David Alan Grier. Also in 2012, Miller created / executive produced (with Russell Brand), Brand X With Russell Brand for FX. In its second season BrandX became FX's first weekly live series (also directed by Miller).