She was born on June 29, 1915, in Saint Joseph, Missouri. By writing an essay in high school called Prevention and Cure of Tuberculosis, Warrick won a contest to be Miss Jubilesta, Missouri's paid ambassador to New York City. Popular legend says that she made her debut in New York on the steps of New York's city hall with an armful of turkeys for Mayor La Guardia.

Warrick began her career in the 1940s as a radio singer where she met her first husband Eric Rolf, but her first big break was being hired by a young Orson Welles for his film Citizen Kane, where she played his first wife, "Emily Monroe Norton". When she auditioned for the part, she read with Welles. She said that because she was so new to the acting business, she was not aware that it was very rare to actually read with the star. What she also didn't realize was that this was also Welles' first film role. Kane proved to be a major moment of her life and the long term success of the film would follow her for the rest of her life.

She celebrated her 80th birthday by attending a special screening of Citizen Kane to a packed, standing room only audience, to which she spoke after the screening. Over the years she collected several books about Orson Welles and Citizen Kane, in which she would write Property of Ruth Warrick, Mrs. Citizen Kane. It was during the filming of Citizen Kane that she learned she was pregnant with her first child, Karen Rolf. Her son, Jon Rolf, was born 16 months later.

The controversy surrounding Citizen Kane led to the film being a box office disaster and Welles, despite co-winning an Academy Award for the screenplay, being shunned by Hollywood. Nevertheless, Welles hired her again for his film Journey Into Fear alongside fellow Kane actor Joseph Cotten. She worked alongside Douglas Fairbanks, Jr., in the film The Corsican Brothers and had a role in the Academy Award winning Disney film Song of the South; she also appeared in Daisy Kenyon, which starred Joan Crawford and Henry Fonda, but by the late 1940s her film roles were becoming infrequent and less notable.

In the 1950s she befriended soap opera inventor Irna Phillips and her protégé, Agnes Nixon. Warrick became a cast member on the soap opera The Guiding Light, playing nurse Janet Johnson from 1953-1954. Phillips was impressed by Warrick's performance and hired her as a cast member on her new soap opera, As The World Turns when the show debuted in 1956. Her character, Edith Hughes, was madly in love with a married man, Jim Lowell. Phillips wanted the characters to live happily ever after, but Procter & Gamble, which owned the show, demanded that the characters be punished for their adultery, so Jim died. Warrick stayed on the show until 1960 and was so popular with fans that she would return several times for holiday visits.

From 1959-1960 she was Una Merkel and future All My Children ("AMC") co-star Eileen Herlie's understudy in the Broadway production of Take Me Along.

During the 1961-62 television season, she starred in the Father of the Bride television series. Then in 1965 she joined the cast of the primetime soap opera, Peyton Place, playing Hannah Cord. While there had been previous primetime soaps (such as One Man's Family), none had enjoyed the phenomenal success of Peyton Place, garnering a new respect for the form that helped to pave the way for shows like Dallas and Dynasty. Warrick received an Emmy Award nomination for this show in 1967, the same year she exited the show. Peyton Place was cancelled two years later.

In 1969, she made her last major film, Disney's The Great Bank Robbery.