The shift of the fruit fly Rhagoletis pomonella (Walsh) in the mid-1800s from downy hawthorn, Crataegus mollis (Torrey & Asa Gray) Scheele, to introduced domesticated apple, Malus domestica (Borkhausen), in the eastern USA is a model for ecological divergence with gene flow. A similar system may exist in the northwestern USA and British Columbia, Canada, where Rhagoletis indifferens Curran (Diptera: Tephritidae) attacks the native bitter cherry Prunus emarginata (Douglas ex Hooker) Eaton (Rosaceae). Populations of R. indifferens have shifted and became economic pests on domesticated sweet cherry, Prunus avium (L.) L., shortly after sweet cherries were introduced to the region in the mid-1800s. The fruiting phenologies of the two cherries differ in a similar manner as apples and hawthorns, with domesticated sweet cherries typically ripening in June and July, and bitter cherries in July and August. Here we report, however, little evidence for genetic differentiation between bitter vs. sweet cherry populations of R. indifferens or for pronounced genetic associations between allele frequencies and adult eclosion time, as has been documented for apple and downy hawthorn flies. The current findings support a previous more geographically limited survey of R. indifferens in the province of British Columbia, Canada, and an analysis of its sister species, R. cingulata, in the state of Michigan, USA, implying a lack of host-related differentiation for flies infesting different cherry host plants. Possible causes for why host races are readily genetically detected for R. pomonella but not for R. indifferens are discussed.