Hamiltonella defensa is well known for its protective roles against parasitoids for its aphid hosts, but its functional roles in insect‐plant interactions are less understood. Thus, the impact of H. defensa infections on life‐history characters and the underlying genetic variation for the grain aphid, Sitobion avenae (Fabricius), was explored on three plants (i.e., wheat, oat, and rye). Compared to cured lines, H. defensa infected lines of S. avenae had lower fecundity on wheat and oat, but not on rye, suggesting an infection cost for the aphid on susceptible host plants. However, when tested on rye, the infected lines showed a shorter developmental time for the nymphal stage than corresponding cured lines, showing some benefit for S. avenae carrying the endosymbiont on resistant host plants. The infection of H. defensa altered genetic variation underlying its host S. avenea’s life‐history characters, which was shown by differences in heritabilities and genetic correlations of life‐history characters between S. avenae lines infected and cured of the endosymbiont. This was further substantiated by disparity in G‐matrices of their life‐history characters for the two types of aphid lines. The G‐matrices for life‐history characters of aphid lines infected with and cured of H. defensa were significantly different from each other on rye, but not on oat, suggesting strong plant‐dependent effects. The developmental durations of infected S. avenae lines showed a lower plasticity compared with those of corresponding cured lines, and this could mean higher adaptability for the infected lines.Overall, our results showed novel functional roles of a common secondary endosymbiont (i.e., H. defensa) in plant‐insect interactions, and its infections could have significant consequences for the evolutionary ecology of its host insect populations in nature.