Double-strand break repair by recombination requires a homology search. In yeast, induced breaks move significantly more than undamaged loci. To examine whether DNA damage provokes an increase in chromatin mobility generally, we tracked undamaged loci under DNA-damaging conditions. We found that the yeast checkpoint factors Mec1, Rad9, and Rad53 are required for genome-wide increases in chromatin mobility, but not the repair protein Rad51. Mec1 activation by targeted Ddc1/Ddc2 enhances chromatin mobility even in the absence of damage. Finally, the INO80 chromatin remodeler is shown to act downstream from Mec1 to increase chromatin mobility, highlighting an additional damage-related role of this nucleosome remodeling complex.