In the Truman Show, Linney played the seemingly wholesome, fresh-scrubbed wife to Jim Carrey's Truman Burbank.
Hit TV series Tales of the City saw her play the ever-so-sweet Mary Ann Singleton to great effect.
And her best actress nomination in the 2001 Academy Awards - for playing the supposedly straight-laced Sammy in You Can Count On Me - is the official stamp of approval for Linney's ability.
Girl-next-door all-American looks have undoubtedly helped Linney secure such roles. But the actress's background also reveals that her onscreen depth is a characteristic of Linney herself.
Linney, 36, grew up in New York City and was, by her own admission, a quiet child given to day-dreaming - especially at school.
"I was a nice girl, but I was a little eccentric. I created a fantasy world for myself, which included a 'sister' who did all the bad things," she told Movieline magazine in 1996.
"I knew I had more imagination than most people and could understand things at a very deep level, but in the basics, I was far behind."
Linney's father Romulus Linney was an off-Broadway playwright and her mother was a nurse. The couple divorced when Linney was six months old.
Despite her shyness, Linney was drawn into her father's world of performance. While at school, she started to work behind the scenes at a theatre.
She went on to study at Brown University and the respected acting college Julliard. Linney completed her training and got an understudy's job on Broadway in Six Degrees of Separation.
She went on to act opposite Ethan Hawke, Tyne Daly, and Jon Voight in The Seagull. In 1994 she won a Calloway Award for her work in Hedda Gabler.
Gradually, Linney began to move into TV and movies by taking a number of minor roles. She played a teacher in emotional family drama Lorenzo's Oil, starring Susan Sarandon.
Noticed
In 1992, she uttered the immortal two words "Mr President?" in the comedy Dave. The following year Linney began to make her mark when she won a leading role in the controversial PBS miniseries Tales of the City.
The show about life in San Francisco dealt with drugs, sex and homosexuality in the 70s. It was a hit with viewers but was dropped after the first series because it caused too much of a stir.
But Linney pushed on and found herself cast as the lead in A Simple Twist of Fate and Steven Spielberg's gorilla-chasing drama Congo in 1995.
Neither were great successes but in the meantime Linney had come to the attention of Hollywood director Greg Hobbit.
Hobbit was casting for his courtroom thriller Primal Fear, starring Richard Gere and Edward Norton, and asked Linney to play the role of Gere's tough-talking lawyer ex-girlfriend.
Though not a big role, Linney 's performance came to the attention of another director - Hollywood legend Clint Eastwood.
Eastwood chose the actress to play his daughter - another lawyer - in Absolute Power.
Pivotal
But it was the following year that really made a difference to Linney's career with a lead role in The Truman Show.
The film centres around Truman Burbank, a man who has no idea that he lives in a studio with hidden cameras everywhere, and those around him are actors in a TV show.
Linney's role as Truman's wife Meryl - a woman whose sole purpose is to hide the truth from her husband - allowed the actress to make the most of her "butter wouldn't melt" looks.
Varied roles followed, including reprising her part as Mary Ann in More Tales of the City. Yet, her most important role to date - that of Sammy in You Can Count On Me - was waiting around the corner in 2000.
The film is at once an emotional drama and romantic comedy about the conflict between a diametrically opposed sister and brother (played by Mark Ruffalo).
Single mother Linney plays the ordered, conservative sister trying to come to terms with her brother's erratic and spontaneous way of life.
As the action unfolds, it becomes clear that the clean-cut Sammy is not quite as tempered as she seems.
Linney has also recently played Gillian Anderson's two-faced "friend" in The House of Mirth.
But future roles on the cards for Linney look like giving her grittier parts, particularly in supernatural thriller Mothman Prophecies with former co-star Richard Gere.