Threats to several of the world's great animal migrations necessitate a research agenda focused on identifying drivers of their population dynamics. The monarch butterfly is an iconic species whose continental migratory population in eastern North America has been declining precipitously. Recent analyses have linked the monarch decline to reduced abundance of milkweed host plants in the USA caused by increased use of genetically modified herbicide‐resistant crops. To identify the most sensitive stages in the monarch's annual multi‐generational migration, and to test the milkweed limitation hypothesis, we analyzed 22 years of citizen science records from four monitoring programs across North America. We analyzed the relationships between butterfly population indices at successive stages of the annual migratory cycle to assess demographic connections and to address the roles of migrant population size versus temporal trends that reflect changes in habitat or resource quality. We find a sharp annual population decline in the first breeding generation in the southern USA, driven by the progressively smaller numbers of spring migrants from the overwintering grounds in Mexico. Monarch populations then build regionally during the summer generations. Contrary to the milkweed limitation hypothesis, we did not find statistically significant temporal trends in stage‐to‐stage population relationships in the mid‐western or northeastern USA. In contrast, there are statistically significant negative temporal trends at the overwintering grounds in Mexico, suggesting that monarch success during the fall migration and re‐establishment strongly contributes to the butterfly decline. Lack of milkweed, the only host plant for monarch butterfly caterpillars, is unlikely to be driving the monarch's population decline. Conservation efforts therefore require additional focus on the later phases in the monarch's annual migratory cycle. We hypothesize that lack of nectar sources, habitat fragmentation, continued degradation at the overwintering sites, or other threats to successful fall migration are critical limiting factors for declining monarchs.