We present demographic, social, historical and ecological data to challenge the generalization that traditional tenure and fishing taboos constitute cultural adaptations that evolved to prevent over-harvesting of subsistence fisheries in the Pacific. In particular, we re-examine the seminal and widely cited arguments of Johannes (Annual Review of Ecology and Systematics 1978; 9, 349–364), which constructed tenure and taboos primarily as traditional fishery management tools for the entire Pacific region. While it is difficult to disprove Johannes’ logic for some sites, particularly in formerly densely populated parts of Polynesia and Micronesia, our review of data and literature for Melanesia indicate very different origins and functions for these institutions. Our study shows that human population densities in most of the Western Pacific prior to European colonial intrusions were too low to have generated sufficient fishing pressure to drive the evolution of a conservation ethic. Our review for Melanesia shows that customary marine tenure and fishing taboos are primarily designed to manage relationships between social groups, rather than to sustain food security from fisheries. We argue that proper recognition of the cultural role of tenure and taboos is critical to progressing marine resource management in Melanesia.