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Abstract Divergent adaptation to new ecological opportunities can be an important factor initiating speciation. However, as niches are filled during adaptive radiations, trait divergence driving reproductive isolation between sister taxa may also result in trait convergence with more distantly related taxa, increasing the potential for reticulated gene flow across the radiation. Here, we demonstrate such a scenario in a recent adaptive radiation ofRhagoletisfruit flies, specialized on different host plants. Throughout this radiation, shifts to novel hosts are associated with changes in diapause life history timing, which act as “magic traits” generating allochronic reproductive isolation and facilitating speciation‐with‐gene‐flow. Evidence from laboratory rearing experiments measuring adult emergence timing and genome‐wide DNA‐sequencing surveys supported allochronic speciation between summer‐fruitingVacciniumspp.‐infestingRhagoletis mendaxand its hypothesized and undescribed sister taxon infesting autumn‐fruiting sparkleberries. The sparkleberry fly andR. mendaxwere shown to be genetically discrete sister taxa, exhibiting no detectable gene flow and allochronically isolated by a 2‐month average difference in emergence time corresponding to host availability. At sympatric sites across the southern USA, the later fruiting phenology of sparkleberries overlaps with that of flowering dogwood, the host of another more distantly related and undescribedRhagoletistaxon. Laboratory emergence data confirmed broadly overlapping life history timing and genomic evidence supported on‐going gene flow between sparkleberry and flowering dogwood flies. Thus, divergent phenological adaptation can drive the initiation of reproductive isolation, while also enhancing genetic exchange across broader adaptive radiations, potentially serving as a source of novel genotypic variation and accentuating further diversification.