He was known for his roles as Thomas Jefferson in 1776 (1972) and as high school basketball coach and former Chicago Bulls player Ken Reeves in the television show The White Shadow (1978–1981).

In the 1980s, he worked mostly in television, winning a Daytime Emmy Award for the CBS afternoon special The Body Human: Facts for Boys (1980).

[9] A member of the National Honor Society in high school, Howard turned down several offers of basketball scholarships in favor of a more focused academic education.

Howard portrayed several U.S. presidents in the 1975 Broadway musical 1600 Pennsylvania Avenue and appeared as Warren G. Harding in Camping with Henry and Tom in 1995.

[13] On television, Howard appeared as Ken Reeves, a Los Angeles high school basketball coach, in The White Shadow, produced by Bruce Paltrow in 1978.

His other dramatic guest roles included NYPD Blue, The Practice, Boston Legal, Cold Case, Dirty Sexy Money, Eli Stone, Brothers and Sisters, Law & Order: Special Victims Unit, Curb Your Enthusiasm, Fairly Legal, Crossing Jordan, The Closer, Blue Bloods, The Golden Girls, The Office, and 30 Rock.

Numerous dramatic and comedic movie roles followed, including: Otto Preminger's Such Good Friends with Dyan Cannon and Jennifer O'Neill, 1776, The Strange Vengeance of Rosalie, Independence, Second Thoughts, Oscar with Sylvester Stallone in 1991, Ulterior Motives, Clear and Present Danger with Harrison Ford in 1994, The Net with Sandra Bullock in 1995, Tactical Assault, Dreamer: Inspired by a True Story, and In Her Shoes in 2005.

He gave an acclaimed performance as Phelan Beale in the 2009 HBO film Grey Gardens, playing opposite Jessica Lange, for which he received an Emmy Award.

Howard was the author of the 2003 book Act Natural: How to Speak to Any Audience,[15] based on the drama courses he had taught at Harvard University.

[16] In 2000, Howard underwent a kidney transplant; the donor was family friend Jeannie Epper,[17] with whom Linda had worked in the stunt community.

George Clooney, in whose 2007 legal thriller, Michael Clayton, Howard appeared, remembered having met him for the first time, in 1983 at 20th Century Fox, as a fan of The White Shadow.