The RAD51 recombinase assembles as helical nucleoprotein filaments on single-stranded (ss)DNA substrates to mediate homologous DNA recombination (HR) and replication fork protection, processes vital in human cells for the maintenance of genome stability. RAD51 assembly is controlled by two key mediator proteins in eukaryotic organisms – the tumour suppressor, BRCA2, and RAD52. Recent evidence suggests that human RAD52 becomes essential for viability in cancer cells lacking BRCA2, making its activity an attractive target for potential therapeutic strategies. However, the mechanisms by which RAD52 and BRCA2 coordinate RAD51 regulation during HR or replication fork protection remain unclear. Therefore, I sought to elucidate these mechanisms and determine the functional redundancy, if any, between the two proteins. Here, I show that human RAD52 co-localises with the ssDNA-binding protein RPA and RAD51 following ionising radiation (IR)-induced damage. Moreover, RAD52 controls the chromatin recruitment and DNA assembly of RAD51, as well as subsequent HR-mediated DNA repair in BRCA2-deficient cells, but is dispensable for these processes in cells that are heterozygous or wild-type for BRCA2. In contrast, RAD52 protects nascent DNA at reversed replication forks from excessive degradation by the MRE11 endonuclease, not only in BRCA2-deficient cells, but also in cells that are heterozygous or wild-type for BRCA2. Mechanistically, RAD52 affects RAD51 recruitment to perturbed replication forks, and its depletion enhances the formation of DNA double-strand breaks (DSBs) and cell death following replication stress induced by hydroxyurea. Thus, these findings suggest divergent requirements for BRCA2 and RAD52 in the regulation of RAD51 during HR versus replication protection. RAD52 is redundant for RAD51-mediated HR in cells that are heterozygous or wild-type for BRCA2, but becomes an essential recombination mediator in cells lacking BRCA2. On the contrary, during replication protection, RAD52 activity is essential for RAD51 regulation regardless of BRCA2 function. Lastly, I describe preliminary results from collaborative experiments deploying electron cryo-microscopy to determine structural mechanisms underlying the regulation of RAD51 filament assembly by BRCA2. A high-resolution structure from a complex of RAD51, ssDNA and the BRC repeats of BRCA2 suggests that BRCA2 BRC repeats may promote conformational changes assisting in homologous DNA strand-pairing. Collectively, the research reported in my thesis provides new insight into the mechanisms by which BRCA2 and RAD52 regulate the RAD51 recombinase during reactions that lead to HR and replication fork protection.