Significance Deficiencies in genome maintenance genes (so-called mutator genes) result in increased mutagenesis that impacts cell evolvability. How the mutational processes drive the evolution of genome structure is not well understood. Here, we used high-throughput sequencing to characterize the mutation events (from punctual mutations to large chromosomal rearrangements) that occurred in mutation accumulation lines derived from a broad set of yeast mutator strains. Establishing genome-wide mutation profiles revealed that each mutator exhibits a unique and sometimes complex mutational signature. Our results also show how the dynamics of mutation accumulation can generate different genomes.