The importance and prevalence of recent ice‐age and post‐glacial speciation and species diversification during the Pleistocene across many organismal groups and physiographic settings are well established. However, the extent to which Pleistocene diversification can be attributed to climatic oscillations and their effects on distribution ranges and population structure remains debatable. In this study, we use morphologic, geographic and genetic (RADseq) data to document Pleistocene speciation and intra‐specific diversification of the unifoliolate‐leaved clade of Florida Lupinus, a small group of species largely restricted to inland and coastal sand ridges across the Florida peninsula and panhandle. Phylogenetic and demographic analyses alongside morphological and geographic evidence suggest that recent speciation and intra‐specific divergence within this clade were driven by a combination of non‐adaptive allopatric divergence caused by edaphic niche conservatism and opportunities presented by the emergence of new post‐glacial sand ridge habitats. These results highlight the central importance of even modest geographic isolation and short periods of allopatric divergence following range expansion in the emergence of new taxa and add to the growing evidence that Pleistocene climatic oscillations may contribute to rapid diversification in a myriad of physiographic settings. Furthermore, our results shed new light on long‐standing taxonomic debate surrounding the number of species in the Florida unifoliate Lupinus clade providing support for recognition of five species and a set of intra‐specific variants. The important conservation implications for the narrowly restricted, highly endangered species Lupinus aridorum, which we show to be genetically distinct from its sister species Lupinus westianus, are discussed.