Two scenarios may explain the origin of sympatric insect host races onto geographically widespread alternate host plants. A single host shift may be followed by range expansion of already specialized populations. Alternately, an ancestral lineage could have colonized multiple locations and at some locations there were independent host shifts. Pea aphid host races on alfalfa and clover have recently expanded their range across Europe and into North America. The population structure of pea aphids was investigated using amplified fragment length polymorphisms (AFLPs) and nuclear sequence-based markers. Neighbor-joining and Bayesian analysis of population structure both provide evidence of a main divergence of aphids on alfalfa and clover. However, aphid populations group by location in both western North America and Sweden, suggesting either independent host shifts and parallel evolution of specialization, or ongoing gene flow at these locations.