Hybrids with different combinations of traits can be used to identify genomic regions that underlie phenotypic characters important to species identity and recognition. Here, we explore links between genomic and plumage variation in Blue-winged Warbler x Golden-winged Warbler (Vermivora cyanoptera x V. chrysoptera) hybrids, which have traditionally been categorized into 2 discrete types. “Lawrence's” hybrids are yellow overall, similar to Blue-winged Warblers, but exhibit the black throat patch and face mask of Golden-winged Warblers. “Brewster's” hybrids are similar to Golden-winged Warblers, but lack the black throat patch and face mask, and sometimes have yellow on their underparts. Previous studies hypothesized that (1) first generation hybrids are of the Brewster's type and can be distinguished by the amount of yellow on their underparts, and that (2) the throat patch/mask phenotype is consistent with Mendelian inheritance and controlled by variation in a locus near the Agouti-signaling protein (ASIP) gene. We addressed these hypotheses using whole genome re-sequencing of parental and hybrid individuals. We found that Brewster's hybrids had genomic hybrid index scores indicating this phenotype can arise by majority ancestry from either parental species, that their plumage varied in levels of carotenoid pigmentation, and individuals captured in multiple years grew consistently less yellow over time. Variation in carotenoid pigmentation showed little relationship with genomic hybrid index score and is thus inconsistent with previous hypotheses that first generation hybrids can be distinguished by the amount of yellow in their plumage. Our results also confirm that variation near ASIP underlies the throat patch phenotype, which we refined to an ∼10–15 Kb region upstream of the coding sequence. Overall, our results support the notion that traditional categorization of hybrids as either Lawrence's or Brewster's oversimplifies continuous variation in carotenoid pigmentation, and its inferred underlying genetic basis, and is based primarily on one discrete trait, which is the throat patch/mask phenotype.