According to the traditional view, RNA-DNA hybrids are major internal threats to genome stability within the cell. Recent studies, however mildly exonerated these hybrid structures by identifying several physiological roles for RNA-DNA hybrids, including regulation of gene expression, transcription termination and DNA replication. Our laboratory showed that transient RNA-DNA hybrids are also required for efficient double-strand break (DSB) repair, and the simultaneous deletion of both RNase H1 and RNase H2 genes fully blocks the Homologous Recombination (HR)-mediated DSB repair pathway. While the roles of RNase H1 and H2 in resolving RNA-DNA hybrids are redundant during DSB-repair, RNAse H2 has an additional role in single base excision repair by recognising and removing mis-incorporated ribonucleosides from the genome. In addition, deletion of RNase H genes leads to widespread accumulation of R-loops throughout the genome, a phenotype that was associated with genomic instability and increased occurrence of DSBs. To better understand the complex role of RNase H enzymes in genome stability and DNA repair, we used RNAse H1- and H2-deficient fission yeast strains and directly measured the mutation rate of these strains with or without additional DNA damage by MMS treatment. By cataloguing SNPs, INDELs and copy number variations after ~1000 generations, and comparing to genome-wide R-loop maps of the mutant and WT strains, we concluded that increased R-loop accumulation likely does not translate to an increased mutation rate in S. pombe cells. Our results call into question the long-standing view that R-loops are detrimental to genomic stability, thus redeeming the negative “reputation” that these RNA-DNA hybrid structures have previously had.