Today’s oceans are undergoing rapid and unprecedented changes resulting from anthropogenic impacts. The North Atlantic right whale, one of the most endangered baleen whales with just over 500 animals remaining in the species, is one example of a species at risk resulting from human influence. Modern right whale research is focused on elevated mortality rates due to vessel collisions and fishing gear entanglement. Although understudied, depressed calving rates also contribute significantly to slow growth. Here we analyze the effect of climate-driven fluctuations in prey abundance on right whale reproductive dynamics since 1980. Calanus finmarchicus, the lipid-rich copepod that right whales prey on, were anomalously abundant in the 1980s and 2000s, while concentrations were low in the 1990s. These fluctuations in copepod abundance were driven remotely by freshwater pulses from the Arctic Ocean, and by changes in advective supply to the Gulf of Maine related to North Atlantic circulation patterns. Synchronized with the low prey regime, right whale calf production in the 1990s was depressed relative to the surrounding decades. In a series of matrix population models, physical variables tied to basin-scale oceanographic mechanisms, climate indices and Continuous Plankton Recorder-derived C. finmarchicus abundance anomalies were tested in the prediction of right whale calf births over the time series 1980-2007. While several lagged physical variables and the annual C. finmarchicus anomaly outcompeted the prey-independent calf prediction model, the best reproduction model was driven by a combination of bimonthly anomalies in sub-regions spanning the southern Gulf of Maine. The objectively-selected regions and seasons of prey anomalies driving the best reproduction model correspond well with known right whale feeding and breeding habits.