After training at the École nationale supérieure des arts appliqués et des Métiers d'arts (school of arts and design) – Olivier de Serres, and at the Conservatoire national supérieur d'art dramatique (National Conservatory of Dramatic Arts of Paris), Éric Ruf joined the Comédie-Française on September 1, 1993, was appointed as the 498th sociétaire on January 1, 1998 and became honorary sociétaire on December 24th, 2014. He has been the General Administrator of the Comédie-Française since August 2014.

On stage, he worked under the direction of Jacques Lassalle, Patrice Chéreau, Denis Podalydès, Christian Schiaretti, Anatoli Vassiliev, Yves Beaunesne, Éric Vignier, Jean-Pierre Vincent, Jean-Luc Boutté, Jean Dautremay, etc.
He played the role of Christian in Rostand’s Cyrano de Bergerac staged by Denis Podalydès, of Brel in Trois hommes dans un salon staged by Anne Kessler, and of Achilles in Kleist’s Penthesilea staged by Jean Liermier.
As Emilie Valatin’s artistic collaborator, he designed the set of da Silva’s Life of the Great Don Quixote de la Mancha and of the Fat Sancho Panza staged by Émilie Valantin.

On the big screen and on television, he worked under the direction of Yves Angelo, Nicole Garcia, Bruno Nuytten, Nina Companeez, Serge Frydmann, Claire Devers, Olivier Pancho, Josée Dayan, and Éric Forestier, etc.

As an artistic director of Edvin(e) company, he co-wrote and directed Du désavantage du vent (Les Solitaires Intempestifs Editions) and Les belles endormies du bord de scène and Armen by Jean-Pierre Abraham.
At the Studio-Théâtre, he staged Et ne va malheurer de ton malheur ma vie, an adaptation of Robert Garnier’s tragedies.

For the opera, he staged and created the scenography of Récit de l'an Zéro by Maurice Ohana and of L'Histoire de l'an Un by Jean-Christophe Marti. He further staged and designed the scenography during a workshop on Christoph Willibald Gluck for Atelier Lyrique of the Paris National Opera, taught at the Cours Florent and at the Conservatoire national supérieur d'art dramatique (National Conservatory of Dramatic Arts of Paris).

He designed sets for Edmond Rostand’s Cyrano de Bergerac, for Molière’s The Misanthrope and for Victor Hugo’s Lucrezia Borgia at the Comédie-Française and for Le Mental de l'équipe by Emmanuel Bourdieu both staged by Denis Podalydès.
Awarded the Prix Gérard-Philipe de la Ville de Paris, he further won, in 2007, two Molière Awards for Best Stage Design/Set and Best Supporting Actor in Cyrano de Bergerac.