Histone chaperones bind to the abundant, basic, and hydrophobic histone proteins to prevent them from forming inappropriate interactions prior to their assembly into nucleosomes. However, chaperones also promote the assembly of nucleosomes. Structural, biochemical, and genetic results reveal how the essential histone chaperone FACT interacts with the four core histones, uncovering unexpected mechanisms for chaperone function, a previously unknown interaction motif for binding H2A-H2B dimers, and the surprisingly dynamic nature of the nucleosome itself.