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At the Sarah Siddons Society's annual banquet, imperious theater critic Addison DeWitt, playwright Lloyd Richards and his wife Karen, producer Max Fabian and legendary actress Margo Channing watch as Eve Harrington is presented with the theater's most prestigious award. Karen recalls when Eve first entered their lives: On a rainy October night, Karen arrives at the theater where Margo is starring in Lloyd's play, and is approached by Eve, who has been to every performance.
Touched by the young woman's devotion to Margo, Karen brings her backstage. In Margo's dressing room, Eve describes her childhood in the Midwest and her marriage to Eddie, an Air Force radio technician who was killed in the war. Eve explains that her life changed when she happened to see Margo in a play in San Francisco, and when the production moved to New York, Eve followed. Director Bill Sampson, Margo's younger boyfriend, comes to say goodbye before leaving for Hollywood to direct a film. Eve accompanies Margo and Bill to the airport, and so endears herself to them that Margo moves Eve into her guestroom. Eve quickly makes herself indispensable as Margo's assistant, to the displeasure of Margo's maid, retired vaudevillian Birdie Coonan. Their relationship becomes strained, however, when Eve arranges a homecoming birthday party for Bill without telling Margo. The night of the party, Margo and Bill quarrel about Eve, and he chides Margo for her jealousy and insecurity about her age.
The tension between them escalates as the guests begin to arrive, and Margo gets drunk and grows maudlin. Max takes Margo aside and says he has foolishly agreed to audition Addison's date, the breath-taking Miss Casswell, and Margo promises to read with her. She then asks Max to give Eve a job in his office. Meanwhile, Eve tells Karen that she would like to replace Margo's pregnant understudy, and Karen promises to speak to Max.
On the day of Miss Casswell's audition, Margo shows up late and encounters Addison in the lobby of the theater. Addison tells her that Miss Casswell already read with Margo's new understudy, Eve, adding that Eve performed brilliantly. Margo argues bitterly with Lloyd and accuses Bill of rehearsing Eve on the sly. When they are alone, Bill asks Margo to marry him, as he has many times before, and when she says no, he walks out. Lloyd goes home and raves to Karen about Eve's performance, and comments that he longs to see Margo put in her place. Recalling that they are scheduled to spend the weekend in the country with Margo, Karen comes up with an idea to teach Margo a lesson, and places a call to Eve. At the end of a tense weekend, Lloyd and Karen are driving Margo to the train station when the car suddenly runs out of gas. While Lloyd sets off to find help, Margo apologizes to Karen for her recent bad behavior and Karen looks guilt-stricken. Eve goes on in Margo's role that night, with Addison and several other critics in attendance, all of them invited that afternoon. After the show, Addison goes backstage and overhears Eve making a play for Bill in her dressing room.
When Bill rejects her, Addison comes in and offers to help promote her career. The next day, Addison's column sings Eve's praises and makes snide remarks about "mature" actresses playing youthful roles. Bill returns to Margo's side to comfort her. Later, Lloyd tells Karen that he would like to put his next play into production right away, with Eve as "Cora," the role that was to have been Margo's. That night, after the show, Lloyd and Karen join Bill and Margo at the Cub Room, and Bill announces that he and Margo are engaged. The waiter brings an urgent note from Eve, asking Karen to meet her in the ladies' room. Eve asks for the lead in Lloyd's new play, adding that Addison will print the truth about Margo's missed performance if her demand is not met. Karen shakily returns to the table, only to hear Margo declare that she does not want to play "Cora." On the night of the play's New Haven opening, Eve tells Addison that Lloyd is going to leave Karen and marry her.
To Eve's surprise, Addison coldly vetoes her plans, saying he has uncovered her scandalous past, and that Karen told him about Eve's attempt to blackmail her. Addison tells her that she belongs to him, and Eve wretchedly submits. Back at the awards banquet, Eve gives a humble acceptance speech and promises to return to the theater after her upcoming assignment in Hollywood. After the banquet, Eve is tired and depressed, and returns to her apartment, where she finds a young woman, Phoebe, waiting in her room. Phoebe says she is the president of one of Eve's fan clubs and took the subway from Brooklyn in the hope of meeting her idol. When the doorbell rings, an exhausted Eve asks Phoebe to take care of things. Phoebe opens the door to Addison, who has brought Eve's award, which was left in the taxi, and takes it into the bedroom. Fondling the award with a determined gleam in her eye, Phoebe tries on Eve's cape and stands before the mirror, posing and bowing.