Major landmarks of developmental processes are often highly conserved across phylogeny, e.g., stages of embryogenesis within phyla. This is largely true for arthropods, with a notable exception; many species interrupt the ‘typical’ developmental process when they enter dormancy or diapause. This trait is highly evolutionarily labile, evolving repeatedly and occurring at different developmental stages in different taxa. Previous studies show that clear instances of repeated evolution result in highly divergent diapause phenotypes. However, there are groups of closely related taxa within which the diapause phenotype appears to be phenotypically conserved, consistent with single evolutionary origins. Such is the case for pupal diapause in the Rhagoletis genus (Diptera: Tehpritidae); nearly all described members have a single generation per year and overwinter as diapausing pupae just prior to molt into the pharate adult. Here we present results that genetically differentiated populations within Rhagoletis pomonella show highly conserved transcriptomic trajectories during diapause. However, Rhagoletis cerasi, a more distantly related species (~5 mya) with a nearly identical diapause life history demonstrates highly distinct transcriptomic trajectories compared to R. pomonella. We describe the quantitative evidence supporting this lack of conservation and discuss implications for the evolutionary flexibility of life histories.