Determining the optimal targets of genomic sub-sampling for phylogenomics, phylogeography, and population genomics remains a challenge for evolutionary biologists. Of the available methods for sub-sampling the genome, hybrid enrichment (sequence capture) has become one of the primary means of data collection for systematics, due to the flexibility and cost efficiency of this approach. Despite the utility of this method, information is lacking as to what genomic targets are most appropriate for addressing questions at different evolutionary scales. In this study, first we compare the benefits of target loci developed for deep- and shallow-scales by comparing these loci at each of three taxonomic levels: within a genus (phylogenetics), within a species (phylogeography) and within a hybrid zone (population genomics). Specifically, we target evolutionary conserved loci that are appropriate for deep phylogenetic scales and more rapidly evolving loci that are informative for phylogeographic and population genomic scales. Second, we assess the efficacy of targeting multiple locus sets for different taxonomic levels in the same hybrid enrichment reaction, an approach we term hierarchical hybrid enrichment. Third, we apply this approach to the North American chorus frog genus Pseudacris to answer longstanding evolutionary questions across taxonomic and temporal scales. We demonstrate that in this system the type of genomic target that produces the most resolved gene trees differs depending on the taxonomic level, although the potential for error is substantially lower for the deep-scale loci at all levels. We successfully recover data for the two different locus sets with high efficiency. Using hierarchical data targeting deep and shallow levels, we (a) resolve the phylogeny of the genus Pseudacris and introduce a novel visual and hypothesis-testing method that uses nodal heat maps to examine the robustness of branch support values to the removal of sites and loci; (b) estimate the phylogeographic history of P. feriarum, which reveals five independent invasions of sympatry by this species to form replicated reinforcement contact zones with P. nigrita with ongoing gene flow into sympatry; and (c) quantify with high confidence the frequency of hybridization in one of these zones between P. feriarum and P. nigrita, which is much lower than previously found by microsatellite-based studies. We find that the hierarchical hybrid enrichment approach offers an efficient, multi-tiered data collection method for simultaneously addressing questions spanning multiple evolutionary scales.