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Abstract Bumble bees (Bombus) exhibit exceptional diversity in setal body color patterns, largely as a result of convergence onto multiple Mullerian mimicry patterns globally. When multiple species cross the same sets of mimicry complexes, they can acquire the same color polymorphisms, providing replicates of phenotypic evolution. This study examines the genetic basis of parallel color pattern acquisition in three bumble bee taxon pairs in western North America that shift between orange-red and black mid-abdominal segmental coloration in Rocky Mountain and Pacific Coastal mimicry regions: polymorphic Bombus vancouverensis and B. melanopygus, and sister species B. huntii and B. vosnesenskii. Initial gene targets are identified using a genome-wide association study, while cross-developmental transcriptomics reveals genetic pathways leading to final pigmentation genes. The data show all three lineages independently target the regulatory region of a segmental-fate determining Hox gene, Abdominal B (Abd-B), for this color transition. For B. vancouverensis and B. melanopygus, this involves different deletions in the same location, and all mimicry pairs differentially express Abd-B and ncRNAs in this locus. Transcriptomics reveals a shared core gene network across species, where Abd-B interacts with nubbin and pigment enzyme ebony to decrease black melanin production in favor of paler, redder morphs. Expression of multiple genes in the melanin biosynthesis pathway is modified to promote this phenotype, with differing roles by taxon. Replicated morphologies unveil key genes and a Hox gene hotspot, while enabling evolutionary tracking of genetic changes to phenotypic changes and informing how gene regulatory networks evolve.