Trained at the Conservatoire national supérieur d'art dramatique (National Conservatory of Dramatic Arts of Paris) in the class of Louis Seigner, Claire Vernet joined the Comédie-Française on September 1, 1964, and became its 453rd sociétaire on January 1, 1975 before being appointed as a sociétaire honoraire in 2002.

She enacted great roles of both the classic and modern repertoire performing in plays by Molière, Marivaux, de Musset, Shakespeare, Guitry, Feydeau, Gogol, Goldoni, Grumberg, Stoppart and Pinter, etc., as well as worked under the direction of Jean Meyer, Jean-Louis Barrault or Jacques Charon. In 1982, she played the roles of Isabel in Witold Gombrowicz’s Ivona, Princess of Burgundia staged by Jacques Rosner at the Théâtre national de l'Odéon, of Anna in Harold Pinter’s Old Times staged by Jean-Pierre Miquel at Petit Montparnasse Theater in 1987, of Arsinoé in Molière’s The Misanthrope staged by Simon Eine in 1990, and of Béline in Molière’s The Imaginary Invalid put on stage by Gildas Bourdet in 1991.
She has also performed the role of Béatrice in Carlo Goldoni’s La Serva amorosa (The Loving Maid) staged by Jacques Lassalle in 1992, and that of Mrs Sørbyin Henrik Ibsen’s The Wild Duck directed by Alain Françon in 1993. Furthermore, she appeared in Georges Feydeau’s Occupe-toi d'Amélie in a staging by Roger Planchon and in Marivaux’s Double Inconstancy (La Double inconstance) directed by Jean-Pierre Miquel in 1995. She performed in Tom Stoppard’s Arcadia, staged by Philippe Adrien, in Molière’s Les Femmes savantes directed by Simon Eine in 1998, in Nikolai Gogol’s The Government Inspector (The Revizor) put on stage by Jean-Louis Benoît in 1999, and in Jean-Claude Grumberg’s Amorphe d'Ottenburg directed by Jean-Michel Ribes in 2000.

During the 2002/2003 season, she was selected by director Nicolas Lormeau for his staging of Geroges Courteline’s Un client sérieux. Bernard Murat cast her in Sacha Guitry’s Le Nouveau Testament in 2003, and Jacques Échantillon selected her for George Feydeau’s Le Mariage de Barillon (The Marriage of Barillon) at the Théâtre du Palais Royal in 2005. In 2006 and 2007, she appeared in Edouard Bourdet’s_Les Temps difficiles_ directed by Jean-Claude Berutti and she performed, in 2009, in Philip Barry’s The Philadelphia Story (Vie privée) under the direction of Pierre Laville at the Théâtre Antoine.

In the movies, she made appearances in_Faustine and the Beautiful Summer,_ a movie by Nina Companeez (1972), in The Parisian Life (La Vie parisienne) by director Christian-Jaque (1977), in À nous les garçons by Michel Lang (1985), in Mikael Buch’s short movie La Déchirure (2007), as well as in Olivier Van Malderghem’s Rondo and François Ozon’s The Refuge (2010).