He is the recipient of numerous awards from organizations including the American Academy of Arts and Letters, National Endowment for the Arts, New York State Council on the Arts and the Tiffany Foundation. He has had over fifty one-person exhibitions in museums and galleries throughout the United States and Europe. His work is in the permanent collections of more than thirty museums, including the Whitney Museum of America Art, the Museum of Fine Arts in Boston, the Museum of Modern Art in New York and the Metropolitan Museum of Art. He served as President of the National Academy of Design from 2001-2005. He is a founding board member of the CUE Art Foundation and served as the CUE Art Foundation's Curator Governor from 2002 to 2015. Amenoff has taught at Columbia for twenty years, where he holds the Eve and Herman Gelman Chair of Visual Arts and was Chair of the Visual Arts Division from 2007-2013.