Natural phenotypic radiations, with their high diversity and convergence, are well-suited for informing how genomic changes translate to natural phenotypic variation. New genomic tools enable discovery in such traditionally nonmodel systems. Here, we characterize the genomic basis of color pattern variation in bumble bees (Hymenoptera, Apidae, Bombus), a group that has undergone extensive convergence of setal color patterns as a result of Müllerian mimicry. In western North America, multiple species converge on local mimicry patterns through parallel shifts of midabdominal segments from red to black. Using genome-wide association, we establish that a cis-regulatory locus between the abdominal fate-determining Hox genes, abd-A and Abd-B, controls the red–black color switch in a western species, Bombus melanopygus. Gene expression analysis reveals distinct shifts in Abd-B aligned with the duration of setal pigmentation at the pupal–adult transition. This results in atypical anterior Abd-B expression, a late developmental homeotic shift. Changing expression of Hox genes can have widespread effects, given their important role across segmental phenotypes; however, the late timing reduces this pleiotropy, making Hox genes suitable targets. Analysis of this locus across mimics and relatives reveals that other species follow independent genetic routes to obtain the same phenotypes.