From his guest-star turns on ER and The Shield, where he played obsessive and violent men, to his 2006 Oscar-winning performance in The Last King of Scotland as ruthless Ugandan dictator Idi Amin, the 49-year-old actor has distinguished himself as a fearsome, shape-shifting force on the big and small screen.
Now he has taken what appears to be an odd fit: a TV drama where he plays the good guy.
In this "against type" role, Whitaker is the lead in Criminal Minds: Suspect Behavior, a spin-off of the successful drama focusing on a team of FBI profilers who travel the country investigating horrific crimes.
"This is a new situation for me," he admitted as he sat in his darkened office at Walt Disney Studios.
"I'm not used to being in just one place - I'm more like a gypsy, going from place to place.
"But I really like this character and I realised what I could do with him."
Showcasing an Oscar winner in prime time is a major coup for any line-up.
"We started out thinking, `You think Forest Whitaker could be interested in this?', and to actually get him on the show is beyond amazing," said Criminal Minds executive producer Edward Allen Bernero, who is also leading the team producing the spin-off. "It helps define what this show is - like Criminal Minds, it's not a procedural. It's all about character."
The dynamics of the two shows, Mr Bernero added, are very different. The team in Criminal Minds: Suspect Behavior has its own problems: "This is a new family, and they are a lot more damaged. [Whitaker's character] Cooper is also damaged. They all support each other."
In person, the 1.85m actor, dressed in a sweatshirt and black pants that camouflage his size, is still formidable, though it is obvious he has slimmed down from what audiences may remember from his portrayals of the British soldier in The Crying Game, jazz legend Charlie Parker in Bird, or the pigeon-loving hitman in Ghost Dog: Way of the Samurai.
He is soft-spoken and thoughtful, in sharp contrast to his often volcanic outbursts on-screen.
It's that subtle internal tension that animates Whitaker's portrayal of Special Agent Sam Cooper, the leader of a special group of agents inside the FBI's Behavioural Analysis Unit.
Cooper maintains a quiet, spiritual approach as he strives to understand the mind of his psychopath suspects.
"Playing someone like Sam is at the source of what I'm always trying to do in my work," Whitaker said.
"He is a leader who thinks everyone has a light inside of them, no matter what kinds of horrible things they are capable of. I'm always interested in human nature. He wants to heal those who come in contact with this darkness."
His talent for delving into and understanding the dark side can be disconcerting to his on-screen co-workers. In the second episode, a local detective teamed with the BAU to track down a suspect who is mutilating victims doesn't approve of the unusual method.
"You have to know them," declares Cooper. "You can't be afraid. Just because I choose to walk in their worlds doesn't mean I have to stay there."
Though a weekly TV series marks a new path for him, Whitaker is no stranger to taking unexpected steps. The actor, not noted for his comedic talents, memorably hosted Saturday Night Live in 2007, and in one skit played a waiter who could not stop singing.
The actor has also achieved success behind the scenes: directing the black female-bonding movie Waiting to Exhale in 1995, and executive-producing Brick City, a Sundance Channel docu-series about a gritty community in Newark, New Jersey.
The often demanding schedule imposed by a TV series has meant some adjustments for Whitaker.
"It was a challenge at first trying to find that rhythm with the writers that would make me feel good," he said.
"We've really developed that now. It feels good."
Playing his Criminal Minds character Cooper fits nicely with his philosophy of creativity.
"I have a discipline about trying to do work that is truthful," he said.
"I was always fortunate enough to play interesting characters, and I've always gone by my heart."
• Criminal Minds: Suspect Behavior premieres Monday at 8.30pm on One.
