The English grain aphid, Sitobion avenae, is a significant agricultural pest affecting wheat, barley, and oats. In Chile, the most prevalent and persistent clone (superclone) of S. avenae harbours the facultative endosymbiont bacterium Regiella insecticola. To determine the role of this bacteria in the ecological success of this superclone, the presence of R. insecticola was manipulated to evaluate the impact on 1) the reproductive performance of this clone in two host plant species (wheat and barley), 2) the production of winged morphs, 3) changes in the proteomic profile of insects, and 4) root/shoot ratio of plant. It was determined that this superclone of S. avenae proliferates differentially in the host plants studied depending on the presence of the facultative bacterial endosymbiont, observing that the clone develops better in wheat when it is infected with R. insecticola while the opposite occurs when it develops in barley. Aphid biomass was higher when harbouring R. insecticola, particularly in barley. Individuals infected with R. insecticola, in both host plants, showed higher proportion of winged individuals. The protein regulation of aphids on wheat was comparatively lower and stable than that on barley. A higher root/shoot biomass ratio was detected in wheat than in oats in plants attacked with aphids harbouring R. insecticola. R. insecticola significantly affects the reproductive and proteomic performance of the S. avenae superclone, changes influenced by the host plant, suggesting that the host plant x facultative endosymbiont interaction can drive host specialization intraclonally, partly the ecological success of the superclones.