Species that share the same ecological niche often avoid costly competition with contextdependent behaviors. This is the case of the invasive insect pest Drosophila suzukii that can develop in ripe fruit where it encounters Drosophila melanogaster . Previous research showed D. suzukii prevents costly larval competition by not ovipositing in substrates with D. melanogaster eggs. We discovered D. suzukii females respond to cues produced by bacteria in the gut microbiome of D. melanogaster . This behavior of D. suzukii varied over time and among populations, revealing subtle condition-dependence. In particular, D. suzukii females that bore D. melanogaster bacteria stopped avoiding sites with D. melanogaster cues. The adaptive significance of the behavior was investigated by reproducing experimentally in-fruit larval competition. D. suzukii larvae only suffered from competition with D. melanogaster if the competitor was associated to its microbiota, suggesting D. suzukii has evolved a solution to avoid offspring develops in challenging environments. We argue that D. suzukii’s competition avoidance behavior has features enabling the design of an evolution-proof repellent to protect crops.