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Abstract Selection causes local adaptation across populations within species and simultaneously divergence between species. However, it is unclear if either the force of or the response to selection is similar across these scales. We show that natural selection drives divergence between closely related species in a pattern that is distinct from local adaptation within species. We use reciprocal transplant experiments across three species ofPhloxwildflowers to characterize widespread adaptive divergence. Using provenance trials, we also find strong local adaptation between populations within a species. Comparing divergence and selection between these two scales of diversity we discover that one suite of traits predicts fitness differences between species and that an independent suite of traits predicts fitness variation within species. Selection drives divergence between species, contributing to speciation, while simultaneously favoring extensive diversity that is maintained across populations within a species. Our work demonstrates how the selection landscape is complex and multidimensional. 

Summary The tree of life is riddled with reticulate evolutionary histories, and some clades, such as the eastern standingPhlox, appear to be hotspots of hybridization. In this group, there are two cases of reinforcement and nine hypothesized hybrid species. Given their historical importance in our understanding of plant speciation, the relationships between these taxa and the role of hybridization in their diversification require genomic validation.Using phylogenomic analyses, we resolve the evolutionary relationships of the eastern standingPhloxand evaluate hypotheses about whether and how hybridization and gene flow played a role in their diversification.Our results provide novel resolution of the phylogenetic relationships in this group, including paraphyly across some taxa. We identify gene flow during one case of reinforcement and find genomic support for a hybrid lineage underlying one of the five hypothesized homoploid hybrid speciation events. Additionally, we estimate the ancestries of four allotetraploid hybrid species.Our results are consistent with hybridization contributing to diverse evolutionary outcomes within this group; although, not as extensively as previously hypothesized. This study demonstrates the importance of phylogenomics in evaluating hypothesized evolutionary histories of non‐model systems and adds to the growing support of interspecific genetic exchange in the generation of biodiversity.