Regiella insecticola has been found to enhance the performance of host aphids on certain plants, but its functional role in adaptation of host aphids to plants is still controversial. Here we evaluate the impacts of R. insecticola infections on vital life-history traits of Sitobion avenae (Fabricius), and their underlying genetic variation and phenotypic plasticity on three plants. It was shown that effects of R. insecticola on S. avenae's fitness (i.e., developmental time and fecundity) were neutral on oat or wheat, but negative on rye. Infections of R. insecticola modified genetic variation that underlies S. avenae's life-history traits. This was demonstrated by comparing life-history trait heritabilities between aphid lines with and without R. insecticola. Moreover, there were enhanced negative genetic correlations between developmental time and fecundity for R. insecticola infected lines, and structural differences in G-matrices of life-history traits for the two types of aphid lines. In R. insecticola-infected aphid lines, there were increases in plasticities for developmental times of first and second instar nymphs and for fecundity, showing novel functional roles of bacterial symbionts in plant-insect interactions. The identified effects of R. insecticola infections could have significant implications for the ecology and evolution of its host populations in natural conditions.