Analyses of population genetic variation in invasive species can provide information on the history of the invasions, breeding systems, and gene flow patterns. We surveyed genetic variation in both social forms of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), throughout the species’ introduced range in the United States, to learn how the unique breeding biology of each form shapes genetic structure at various scales, to discern genetic footprints of the invasion process, and to reconstruct the origin and spread of each form. Consistent with more limited earlier studies, our analyses revealed significant local mitochondrial DNA (mtDNA) differentiation in the polygyne (multiple colony queens) but not in the monogyne (single colony queen) social form as well as pronounced mtDNA differentiation coupled with weaker nuclear differentiation between sympatric populations of the two forms. At a larger scale, we found no mtDNA but significant nuclear regional differentiation. In general, populations were most similar to other populations of the same social form at their mtDNA genomes. These higher level patterns of structure are consistent with the spread of the ant by long-distance, human-mediated dispersal, with subfounder populations of each form typically established by queens of the same form. Bayesian analyses showed that study populations most distant from the claimed site of entry, Mobile, AL, have diverged most from the hypothetical founder population, consistent with an invasion scenario in which the ants spread outward from Mobile through repeated subfounder events. Several lines of evidence raise the possibility of secondary introductions of S. invicta into the United States.