Closely related taxa having undergone rapid evolution and hybridization are often difficult to delimit. Next generation molecular methods combined with bioinformatic tools provide unprecedented opportunities to discern among cryptic taxa and study the complex evolutionary processes underlying the divergence of independent lineages as well as secondary hybridization or gene-flow among them. Having radiated across the Hawaiian archipelago within the past five million years, Polypodium pellucidum encompasses a complex of endemic ferns exhibiting substantial morphological and ecological variation. Using a set of 400 universal fern baits with target-capture, admixture analyses, and phylogenetic methods, we show that P. pellucidum lineages have undergone rapid divergences structured by morphology, ecological niche and island biogeography. We also present evidence for hybridization among lineages, clarifying previous morphological ambiguities and overlap between taxa. Our results offer insights into the co-occurring evolutionary factors structuring divergence and hybridization in P. pellucidum as well as inform conservation of these endemic taxa.