Coexistence of host?specific herbivores on plants is believed to be governed by interspecific interactions, but few empirical studies have systematically unraveled these dynamics. We investigated the role of several factors in promoting coexistence among the aphids Aphis nerii, Aphis asclepiadis, and Myzocallis asclepiadis that all specialize on common milkweed (Asclepias syriaca). Competitive exclusion is thought to occur when interspecific competition is stronger than intraspecific competition. Consequently, we investigated whether predators, mutualists, or resource quality affected the strength of intra? vs. interspecific competition among aphids in factorial manipulations of competition with exposure to predation, ants, and variable plant genotypes in three separate experiments. In the predation × competition experiment, predators reduced aphid per capita growth by 66%, but the strength of intra? and interspecific competition did not depend on predators. In the ants × competition experiment, ants reduced per capita growth of A. nerii and M. asclepiadis (neither of which were mutualists with ants) by approximately one?half. In so doing, ants ameliorated the negative effects of these competitors on ant?tended A. asclepiadis by two?thirds, representing a novel benefit of ant–aphid mutualism. Nevertheless, ants alone did not explain the persistence of competitively inferior A. asclepiadis as, even in the presence of ants, interspecific competition remained stronger than intraspecific competition. In the plant genotype × competition experiment, both A. asclepiadis and M. asclepiadis were competitively inferior to A. nerii, with the strength of interspecific competition exceeding that of intraspecific competition by 83% and 23%, respectively. Yet these effects differed among milkweed genotypes, and there were one or more plant genotypes for each aphid species where coexistence was predicted. A synthesis of our results shows that predators play little or no role in preferentially suppressing competitively dominant A. nerii. Nonetheless, A. asclepiadis benefits from ants, and A. asclepiadis and M. asclepiadis may escape competitive exclusion by A. nerii on select milkweed genotypes. Taken as a whole, the coexistence of three host?specific aphid species sharing the same resource was promoted by the dual action of ants as antagonists and mutualists and by genetic diversity in the plant population itself.