The Enallagma and Lestes damselflies have both diversified and adapted over the past 10–15 million years to the various ecological milieus found along the pond permanence gradient among North American ponds and lakes. Previous articles have explored this diversification process for Enallagma. In this article, we present a phylogenetic hypothesis for the North American Lestes, use this hypothesis to reconstruct Lestes diversification, and compare the diversification processes inferred for Lestes and Enallagma. The results of this study suggest that Lestes began in temporary ponds where large dragonflies are the top predators, while Enallagma began in permanent lakes where fish are the top predators. Starting from these different ancestral habitats, both genera have invaded and adapted to habitats already occupied by the other genus. Moreover, these adaptive habitat shifts involved substantial convergence on the behaviors used to deal with fish and dragonfly predation in both genera and a major life‐history shift from diapausing to directly developing eggs in Lestes. However, in Lestes lineages invading fish lakes, swimming speed and morphology did not change to match those of Enallagma species, illustrating that reciprocal shifts between alternative selection regimes are not necessarily evolutionary opposites. Also, the greater sizes and growth rates of Lestes species compared to Enallagma species, which should impart substantial ecological advantages in competition between the genera, were shown to result from phylogenetic inheritance and not from adaptive diversification. This historical analysis of diversification raises new questions about the relationship between the macroevolutionary mechanisms driving lineage diversification and the ecological mechanisms structuring local food webs and regional species assemblages.