A project Towne had long sought to bring to the screen came to fruition in 2006 with Ask the Dust, a romantic period piece set in Los Angeles based on the acclaimed novel by John Fante and starring Colin Farrell and Salma Hayek. Towne had found the novel while researching Chinatown, looking for material that would honestly describe that particular era of Los Angeles. He became so entranced by the book that he arranged to meet with its author—himself a screenwriter—in person. "I was an unknown," Towne said. "I hadn't written anything of note." But Fante greeted the young fan with accusations like "What makes you think you're any kind of judge of my work?" Ask the Dust received mixed reviews and failed at the box office. The film was entered into the 28th Moscow International Film Festival.
In 2006, Towne was the subject of artist Sarah Morris's film, Robert Towne. Morris describes him as an “elliptical figure” whose career exemplifies a certain characteristic mode of working in the film industry, marked by collaboration, shared or changing roles. Morris's 19,744-square-foot (1,834.3 m) painting installation in the lobby of the Lever House in Manhattan, commissioned by the Public Art Fund, was also titled "Robert Towne".
