Dennison first worked at the Guggenheim as a summer intern of Wellesley College in 1973; in 1978 she began working there independently. She worked as an exhibition coordinator, assistant curator, and deputy director and chief curator. In 2003 she was a candidate for the position of director of the Whitney Museum, but the position went to Adam D. Weinberg.[4]
In October 2005, Dennison became the director of the Guggenheim Museum and replaced seventeen-year director Thomas Krens, as the director of the Solomon R. Guggenheim Foundation. She was also approached by the Los Angeles County Museum of Art and the Cleveland Museum of Art to serve as a director there.[1]
As director of the Guggenheim, Dennison organized 35 shows, one of which was a traveling exhibition of 125 works in the Guggenheim’s collection.[1][5]