The Japanese Murrelet Synthliboramphus wumizusume is a rare, globally ‘Vulnerable’ seabird, endemic to Japan and South Korea. However, little is known of its at-sea distribution, habitat or threats. We conducted several years of at-sea surveys around Japan to model Japanese Murrelet density in relation to habitat parameters, and make spatial predictions to assess the adequacy of the current Japanese marine Important Bird and Biodiversity Area (IBA) network for the species. During a five-year period, 3,485 km of at-sea surveys recorded 3,161 Japanese Murrelets around four breeding locations. Maximum murrelet group size was 90 individuals with a mean group size of 2.9 ± 4.2 individuals. Models of Japanese Murrelet at-sea density around the two largest breeding locations predicted that almost all murrelets occur within 30 km of the breeding colony and most within 10 km. Murrelets were predicted closer to the colony in May than in April and closer to the colony at a neritic colony than at an offshore island colony. Additionally, murrelets breeding on an offshore island colony also commuted to mainland neritic habitat for foraging. The marine habitat used by Japanese Murrelets differed between each of the four surveyed colonies, however oceanographic variables offered little explanatory power in models. Models with colony, month and year generated four foraging radii (9–39 km wide) containing murrelet densities of > 0.5 birds/km2. Using these radii the Japanese marine IBA network was found to capture between 95% and 25% of Japanese Murrelet at-sea habitat while breeding and appears appropriately configured to protect near-colony murrelet distributions. Given the range of marine habitats that breeding murrelets inhabit, our simple models offer an applicable method for predicting to unsampled colonies and generating ecologically-informed seaward extension radii. However, data on colony populations and further at-sea surveys are necessary to refine models and improve predictions.