Large-scale breeding failures, such as offspring die-offs, can disproportionately impact wildlife populations that are characterized by a few large colonies. However, breeding monitoring-and thus investigations of such die-offs-is especially challenging in species with long reproductive cycles. We investigate two unresolved dramatic breeding failures that occurred in consecutive years (2009 and 2010) in a large king penguin Aptenodytes patagonicus colony, a long-lived species with a breeding cycle lasting over a year. Here we found that a single period, winter 2009, was likely responsible for the occurrence of breeding anomalies during both breeding seasons, suggesting that adults experienced poor foraging conditions at sea at that time. Following that unfavorable winter, the 2009 breeding cohort-who were entering the late stage of chick-rearing-immediately experienced high chick mortality. Meanwhile, the 2010 breeding cohort greatly delayed their arrival and egg laying, which would have otherwise started not long after the winter. The 2010 breeding season continued to display anomalies during the incubation and chick-rearing period, such as high abandonment rate, long foraging trips and eventually the death of all chicks in winter 2010. These anomalies could have resulted from either a domino-effect caused by the delayed laying, the continuation of poor foraging conditions, or both. This study provides an example of a large-scale catastrophic breeding failure and highlights the importance of the winter period on phenology and reproduction success for wildlife that breed in few large colonies.