Explaining the coexistence of closely related species sharing a single resource has been a long-standing challenge in ecology. Here we report on studies comparing the aphids Aphis nerii and A. asclepiadis that feed sympatrically on the milkweed Asclepias syriaca in northeastern North America. We sought to identify tradeoffs among species’ attributes that might promote coexistence, but in most instances A. nerii was superior to A. asclepiadis. Aphis nerii was 84% more fecund, fed upon 880% more phloem sap, and was affected 70% less by intraspecific competition as compared to A. asclepiadis. In interspecific competition, A. nerii reduced A. asclepiadis abundance by 77%, whereas A. asclepiadis did not affect A. nerii. In dispersal trials, 10% of winged A. nerii but only 1% of A. asclepiadis successfully moved from non-host plants to A. syriaca. We also investigated whether there were differences in aphid interactions with milkweed cardenolides. Jasmonic acid increased milkweed cardenolides by 33%, a realistic amount similar to that induced by several leaf-chewing herbivores. Nevertheless, jasmonate-induced cardenolides failed to affect aphid performance and aphid feeding had no effect on milkweed cardenolide concentration. Yet cardenolides were important for aphid resistance to predators; A. nerii sequestered 25% more cardenolides and was preyed upon 50% less than A. asclepiadis. Interactions with cardenolides thus again favored A. nerii over A. asclepiadis. Given that A. nerii and A. asclepiadis are decidedly not equivalent in their demography, competitive ability, defense and dispersal, our results strongly refute the notion that neutral processes can explain coexistence of these aphids. Based on field observations, we propose two tradeoffs – timing of milkweed colonization and relationships with ants – as putative mechanisms for the coexistence of these congeners.