The origins and evolution of Hawaiian biodiversity are a matter of controversy, and the mechanisms of lineage diversification for many organisms on this remote archipelago remain unclear. Here we focus on the poorly-known endemic leaf-mining moth genus Philodoria (Lepidoptera, Gracillariidae), whose species feed on a diversity of Hawaiian plant lineages, many of which are critically endangered. We use anchored hybrid enrichment to assemble the first phylogenomic dataset (507 loci) for any Hawaiian animal taxon. To uncover the timing and pattern of diversification of these moths, we apply two frequently used dating calibration strategies, biogeographic calibrations and secondary calibrations. Island calibrations on their own resulted in much younger and unrealistic dates compared to strategies that relied on secondary calibrations. Our dating results indicate that Philodoria is among the oldest known Hawaiian arthropod lineages. Philodoria likely originated on the now partially sunken islands of Laysan or Lisianski, approximately 21 million years ago, and were associated with host plants in the families Ebenaceae, Malvaceae, or Primulaceae. Major feeding groups associated with specific host plant families originated soon after the plants colonize the islands. Allopatric isolation and host shifts, in concert and independently, likely play major roles in the diversification of Philodoria.