Networks of no-take marine reserves (NTMRs) are a widely advocated strategy for managing coral reefs. However, uncertainty about the strength of population connectivity between individual reefs and NTMRs through larval dispersal remains a major obstacle to effective network design. In this study, larval dispersal among NTMRs and fishing grounds in the Philippines was inferred by conducting genetic parentage analysis on a coral-reef fish (Chaetodon vagabundus). Adult and juvenile fish were sampled intensively in an area encompassing approximately 90 km of coastline. Thirty-seven true parent-offspring pairs were accepted after screening 1978 juveniles against 1387 adults. The data showed all types of dispersal connections that may occur in NTMR networks, with assignments suggesting connectivity among NTMRs and fishing grounds (n = 35) far outnumbering those indicating self-recruitment (n = 2). Critically, half (51%) of the inferred occurrences of larval dispersal linked reefs managed by separate, independent municipalities and constituent villages, emphasising the need for nested collaborative management arrangements across management units to sustain NTMR networks. Larval dispersal appeared to be influenced by wind-driven seasonal reversals in the direction of surface currents. The best-fit larval dispersal kernel estimated from the parentage data predicted that 50% of larvae originating from a population would attempt to settle within 33 km, and 95% within 83 km. Mean larval dispersal distance was estimated to be 36.5 km. These results suggest that creating a network of closely spaced (less than a few tens of km apart) NTMRs can enhance recruitment for protected and fished populations throughout the NTMR network. The findings underscore major challenges for regional coral-reef management initiatives that must be addressed with priority: (1) strengthening management of NTMR networks across political or customary boundaries; and (2) achieving adequate population connectivity via larval dispersal to sustain reef-fish populations within these networks.