The apple maggot fly, Rhagoletis pomonella Walsh (Diptera: Tephritidae), is a serious quarantine pest in the apple-growing regions of central Washington and Oregon. The fly is believed to have been introduced into the Pacific Northwest via the transport of larval-infested apples near Portland, Oregon, within the last 40 yr. However, R. pomonella also attacks native black hawthorn, Crataegus douglasii Lindley (Rosales: Rosaceae), and introduced ornamental hawthorn, Crataegus monogyna Jacquin, in the region. It is, therefore, possible that R. pomonella was not introduced but has always been present on black hawthorn. If true, then the fly may have independently shifted from hawthorn onto apple in the Pacific Northwest within the last 40 yr after apples were introduced. Here, we test the introduction hypothesis through a microsatellite genetic survey of 10 R. pomonella sites in Washington and 5 in the eastern United States, as well as a comparison to patterns of genetic variation between populations of Rhagoletis cingulata Loew and Rhagoletis indifferens Curran, two sister species of cherry-infesting flies known to be native to the eastern and western United States, respectively. We report results based on genetic distance networks, patterns of allelic variation, and estimated times of population divergence that are consistent with the introduction hypothesis for R. pomonella. The results have important implications for R. pomonella management, suggesting that black hawthorn-infesting flies near commercial apple-growing regions of central Washington may harbor sufficient variation to utilize apple as an alternate host, urging careful monitoring, and possible removal of hawthorn trees near orchards.