In Saccharomyces cerevisiae, chromosomal mobility increases after the formation of a double-strand break (DSB). Cut loci expand their radius of exploration substantially in a process termed local mobility. In addition, there is an increase in global mobility following a DSB, in which even undamaged loci expand their radius of exploration. Here, we examine the role of the RecA-like recombinase Rad51 in regulating the mobility of chromosomes in diploid budding yeast cells after DSB formation. We find that global mobility is dependent on RAD51 throughout the cell cycle, and that Rad51 regulates mobility in G1 as well as S phase chromosomes. This regulation depends on a functional Walker A ATPase domain, but does not require dsDNA binding or strand exchange activities of Rad51 protein. Although some ssDNA binding is essential for global mobility, extensive filament formation is dispensable, as rad52∆ cells are still capable of promoting increased movement. Finally, we find that DNA damage checkpoint induction is both necessary and sufficient to induce global mobility in diploid cells. Interestingly, this induction, even in undamaged cells, is dependent upon the presence of Rad51. We propose that Rad51 serves as an important damage sensor that signals to the DNA damage checkpoint machinery to promote mobility.