While there he was asked to write a promo for the series The Six Million Dollar Man, which was well liked by the network. Holcomb was hired as associate producer on the series, leading to his hiring as director for several episodes. After the show ended its run, Holcomb directed the original Captain America film in 1979.
Throughout the rest of the 1970s and 1980s, Holcomb primarily directed for television; including Battlestar Galactica, Fantasy Island, Hill Street Blues, The Greatest American Hero, and the pilots of The A-Team, Scarecrow and Mrs. King, The Equalizer, Wiseguy and China Beach. Throughout the 1990s, Holcomb worked almost exclusively in movies for television such as A Promise to Keep (1990), The Prosecutors (1996), Thanks of a Grateful Nation (1998), Songs in Ordinary Time (2000), The Pentagon Papers (2003), Code Breakers (2005), Bounty Hunters (2005), and The Way (2006). He also directed the feature film Chains of Gold in 1991. During the 2000s, Holcomb returned to television series, directing episodes of the series The District, The Education of Max Bickford, The Lyon’s Den, The West Wing, Invasion, Shark, Moonlight, Lost, Numb3rs, NCIS: Los Angeles, Justified, The Good Wife, The Defenders, CSI: Miami, Law & Order: LA, Rizzoli & Isles, Elementary, and Ironside. One of Holcomb’s signature accomplishments is having directed both the pilot and series finale of the long-running medical drama ER.
For his directorial efforts, Holcomb has been nominated for three DGA Awards, winning for the pilot of ER in 1995. He has also been nominated for four Primetime Emmys, winning once for the series finale of ER in 2009. An active member of the Directors Guild, Holcomb served on the National Board from 2003-2013, the Western Directors Council from 1997-2013, the 1996, 1999, 2002, 2005, 2008, 2011, and 2014 Negotiating Committees, and is the co-chair of the Television Creative Rights Committee.