Monarch butterflies and their unique system of multigenerational migration have long fascinated the public, and concerns for the fate of this charismatic insect have grown due to the consistent declines in overwintering colony size over the last 20 years. Risks to this migratory insect have been considered in terms of climate change, habitat and thus population fragmentation, and decreased host plant availability. However, another obvious danger, that of decreased heterozygosity resulting from decreasing population size, has yet to be explored. Here we report experimental evidence for immediate inbreeding depression in individuals from the migratory population. Inbred matings produced less viable eggs and inbred offspring had higher developmental mortality and shorter lifespans. We discuss these results in the context of monarch migration extinction risk and suggest that additional genetic monitoring should be undertaken to protect this iconic animal.