Aging is characterized by genome instability, which contributes to cancer formation and cell lethality leading to organismal decline. The high levels of DNA double-strand breaks (DSBs) observed in old cells and premature aging syndromes are likely a primary source of genome instability, but the underlying cause of their formation is still unclear. DSBs might result from higher levels of damage or repair defects emerging with advancing age, but repair pathways in old organisms are still poorly understood. Here we show that pre-meiotic germline cells of young and old flies have distinct differences in their ability to repair DSBs by the error-free pathway homologous recombination (HR). Repair of DSBs induced by either ionizing radiation (IR) or the endonuclease I-SceI is markedly defective in old flies. This correlates with a remarkable reduction in HR repair measured with the DR-white DSB repair reporter assay. Strikingly, most of this repair defect is already present at 7 days of age. Finally, HR defects correlate with increased amount of Rad51 expression and recruitment to damage in old organisms, suggesting that HR in older flies is defective after Rad51 recruitment. These data reveal that DSB repair defects arise early as the organism ages, and, contrary to previous conclusions, suggest HR defects as a leading cause of genome instability in older animals.