Butterflies and moths (Lepidoptera) are one of the major super-radiations of insects, comprising nearly 160,000 described extant species. As herbivores, pollinators, and prey, Lepidoptera play a fundamental role in almost every terrestrial ecosystem. Lepidoptera are also indicators of environmental change and serve as model organisms for research on mimicry and genetics. They have been central to the development of co-evolutionary hypotheses, such as butterflies with flowering plants, and moths' evolutionary arms race with echolocating bats. However, these hypotheses have not been rigorously tested because a robust lepidopteran phylogeny and timing of evolutionary novelties are lacking. To address these issues, we inferred a comprehensive phylogeny of Lepidoptera, using the largest data set assembled for the order (2,098 orthologous protein-coding genes from 186 species representing nearly all superfamilies), and dated it with carefully evaluated synapomorphy-based fossils. The oldest members of the Lepidoptera crown group appeared in the Late Carboniferous (~300 million years ago [Ma]) and fed on non-vascular land plants. Lepidoptera evolved the tube-like proboscis in the Middle Triassic and the proboscis allowed them to acquire nectar from flowering plants. This key morphological innovation, along with other traits, likely promoted the extraordinary diversification of superfamily-level lepidopteran crown groups. The ancestor of butterflies was likely nocturnal, and our results indicate that butterflies became day-flying in the Late Cretaceous. Moth hearing organs arose multiple times prior to the evolutionary arms race between moths and bats, perhaps initially detecting a wide range of sound frequencies before being co-opted to specifically detect bat sonar.