Two genetically differentiated forms of fall armyworm, Spodoptera frugiperda (J. E. Smith), use different graminaceous host plants, coexist sympatrically throughout their ranges, yet seem to hybridize. To address the taxonomic status of the two forms, determine extent and directionality of hybridization, and examine host specificity, we compiled multilocus genotypes consisting of mitochondrial DNA (mtDNA) haplotypes, an esterase locus, and eight amplified fragment-length polymorphism (AFLP) loci in moths collected across a broad geographic range. Multilocus analyses indicated 16% of individuals sampled were potentially hybrids with a minority being F₁ in origin. Analysis of host use indicated asymmetries in host specificity with one strain specific to corn, Zea mays L., and the other strain predominating on pasture grasses and rice, but occasionally using corn. Location of hybrids in nature was biased toward cornfields, the habitat used by both strains. To assess genetic divergence of each gene, we calculated their relative strain discriminating ability. Eight AFLP loci collectively had the greatest discriminating power (98%), followed by a single AFLP locus (93%) and mtDNA (91%). Esterase exhibited 89% discrimination. Esterase is X-linked along with an assortative mating trait, suggesting esterase differentiation may be maintained by association with strain-specific fitness genes. Despite strong discrimination of these genes, most of the genome surveyed was not distinct. Cytonuclear comparisons provided evidence for unidirectional matings consistent with mate preference studies. Collectively, these data support introgressive hybridization between recently evolved species that are not completely reproductively isolated. Genetic divergence in the presence of gene flow may be a common phase in the speciation process, especially in taxa whose ranges have been altered dramatically by humans.