Human RAD52 is a prime target for synthetic lethality approaches to treat cancers with deficiency in homologous recombination. Among multiple cellular roles, RAD52's functions in homologous recombination repair and stalled replication fork protection appear to substitute for those of the tumor suppressor protein BRCA2. However, the mechanistic details of how RAD52 substitutes for BRCA2 functions are only beginning to emerge. RAD52 forms an oligomeric ring enveloped by ∼200-residue-long disordered regions, forming a highly multivalent and branched protein complex that promotes supramolecular assembly. Here, we demonstrate that RAD52 undergoes homotypic phase separation, forming condensates that recruit key homologous recombination factors, including single-stranded DNA (ssDNA), replication protein A (RPA), and the RAD51 recombinase. Furthermore, we show that RAD52 phase separation is regulated by its interaction partners such as ssDNA and RPA. Through fluorescence microscopy, we observe that RAD52 promotes the formation of RAD51-ssDNA fibrillar structures. To resolve the fine architecture of these fibrils, we employed single-molecule super-resolution imaging via DNA-PAINT and atomic force microscopy, revealing that RAD51 fibrils comprise bundles of individual RAD51 nucleoprotein filaments. Additionally, we show that RAD52 induces end-to-end tethering of RAD51 nucleoprotein filaments. Collectively, these findings highlight distinctive macromolecular organizational features of RAD52 that may underpin its diverse cellular functions.