Decreased reliance on pesticides can be achieved through a clever use of eco-evolutionary knowledge via intercropping economically valuable crops with companion plants that can hamper pest outbreaks. We created a greenhouse multi-layered microcosm system to test two potato peach aphid clones, performing alone or in competition, on mixes of genetically variable cultivars of cabbage, with and without onion. The onion acted as a nuisance/disturbance for the pest, which was generally for the benefit of the cabbage albeit both plants sharing space and nutrients. The onion effect was context-specific and differed by aphid genotype. Onion variable nuisance negatively affected the numbers of one aphid genotype (green) across all contexts, while the other genotype (pink) numbers were decreased in two contexts only. However, the green performed better than the pink on all cases of cabbage di-mixes despite its numbers being capped when the onion was present. Further, there was also a general aphid propensity to wander off the plant along with a differential production of winged morphs to escape the onion-affected environments. Moreover, through a comparative increase in dry mass, which was subject to onion and aphid effects, a diversity effect was found where the cabbages of fully genetically variable microcosms sustained similar final dry mass compared with non-infested microcosms. Our findings provide fresh insights into the use of multi-layered contextual designs that not only allow disentangling the relative effects of genetic variation and modes of interaction, but also help integrate their benefits into pest management in view of companion planting.