Monarch butterflies are known for their spectacular annual migration in eastern North America, with millions of monarchs flying up to 4,500 kilometers to overwintering sites in central Mexico. Monarchs also live west of the Rocky Mountains, where they travel shorter distances to overwinter along the Pacific Coast. Monarch numbers have recently dwindled, and monarch migration may be on the brink of extinction. It is often assumed that eastern and western monarchs form distinct evolutionary units that require specific protection, but genomic studies to support this notion are lacking. We used a tethered flight mill to show that migratory eastern monarchs have greater flight performance than western monarchs. However, analyzing more than 20 million SNPs in 43 monarch genomes, we found no evidence for genomic differentiation between eastern and western monarchs, suggesting the existence of one panmictic migratory population. Our genomic analysis also showed identical and low levels of genetic diversity, and a lack of singleton alleles, indicating a shared history of decline of eastern and western monarchs. Gene expression analysis of a subset of candidate genes during active flight revealed differential gene expression related to non-muscular motor activity. Our results demonstrate that North American monarchs form one panmictic and declining population, and that differences in migration distance and destination are therefore likely driven by environmentally induced differential gene expression. Our study indicates that eastern and western monarchs do not form distinct genetic populations, suggesting that preservation of eastern monarchs could potentially rescue western migration and vice versa.