Deciphering the mechanisms of niche separation between species is a central question in ecology. However, the influence of symbiotic microbes on competitive interactions remains seldom studied. Microbe-mediated niche partitioning may be particularly important in Drosophilid flies, which larvae rely on exo-symbiotic microbes for fruit consumption. We previously demonstrated how the invasive pest Drosophila suzukii facilitates fruit infestation by D. melanogaster through the wounding of fruits by ovipositing females, and the subsequent cultivation of bacteria and yeast by offspring larvae. We now demonstrate that ovipositing D. suzukii females avoid fruits previously exposed to D. melanogaster. Using axenic strains, we further show that microbes carried by D. melanogaster are responsible for this repellency. Additional experiments reveal that the avoidance of D. melanogaster by D. suzukii relies on short-scale taste perception. Comparison among D. suzukii populations indicates the behavior is present in populations from both the native and invasive ranges but depends on previous fly experience. On-going experiments test the hypothesis that D. suzukii females avoid fruits infested by D. melanogaster because its symbionts would create conditions unfavorable for D. suzukii progeny. Our study highlights how symbiotic microbes may determine interspecific interactions and niche partitioning through facilitation and competition; the results further suggest natural repellents may provide innovative and sustainable biocontrol solutions against agricultural pests