During his 30-year career he worked with some of France's greatest directors of the time, including Louis Malle, Claude Chabrol, Jean-Luc Godard, Costa-Gavras, Claude Lelouch and François Truffaut, who gave him two of his most memorable roles, as Fergus in The Bride Wore Black (1968) and as Bertrand Morane in The Man Who Loved Women (1977).

Denner served as a Free French partisan in the Vercors mountains and destroyed a Nazi SS truck with a grenade; he was wounded and later received the Croix de Guerre for this operation.

Two years later, in 1957, he secured another secondary role in Louis Malle's legendary Elevator to the Gallows, alongside Jeanne Moreau, a co-performer of his from the days of the TNP.

In 1962 Jean-Luc Godard wanted to film Jean Giraudoux's play Pour Lucrèce starring Denner along with Sami Frey and Michel Piccoli, but when cast and crew had already been assembled he called off the shoot on the first day of filming after a prolonged downpour caused a long delay.

[2] In 1963 Denner was offered his first leading role by Claude Chabrol in Landru, a film considered by many as his greatest on-screen performance.