Rhagoletis pomonella (Walsh) is an important pest of apples and has been at the center of a long-standing debate concerning modes of speciation. The fly has been proposed to speciate without geographic isolation (i.e., in sympatry) in the process of shifting and adapting to new host plants. Previous studies have shown that diapause-related traits play a key role in adapting apple- and hawthorn-infesting races of R. pomonella to a difference in the fruiting times (phenologies) of their respective host plants. These experiments indicated that prewinter temperature and its duration affected the survivorship and genetics of over-wintering R. pomonella pupae. However, the earlier work did not test whether photoperiod and light intensity, two environmental factors that also differ between the host races, affect the genetics of diapause. Here, we report that variation in photoperiod, but not light intensity, during the larval stage affects adult eclosion. Haw-origin larvae exposed to longer photoperiods (18:6 [L:D] h) eclosed significantly earlier that those experiencing shorter photoperiods (14:10 and 10:14 [L:D] h). We also confirmed previously observed genetic relationships between eclosion time and six allozyme loci displaying allele frequency differences between the haw and apple host races. However, we did not find a significant genetic response to photoperiod for any allozyme. Our results suggest that, while photoperiod cues can regulate R. pomonella diapause, daylength is probably of secondary importance relative to temperature and season length in genetically differentiating the host races.