Understanding population connectivity using molecular markers has broad application in natural resource management. The most popular approach has been indirect estimates of connectivity derived from allele frequencies. More recently, the spatial distribution of parent-offspring and full-sibling (FS) pairs has been used to provide direct estimates of larval or juvenile movements. In combination, these approaches potentially provide contemporary and long-term connectivity estimates. Here we combine indirect estimates from whole mitogenome sequences and nuclear SNPs with direct estimates of adult and juvenile movements from FS and half-sibling (HS) data for the Critically Endangered Speartooth Shark Glyphis glyphis. Over 350 juveniles were captured from the three river systems in tropical northern Australia where this species is found. None of the 72 FS and 24 same-cohort HS pairs of juvenile sharks were captured in different rivers, suggesting strong river fidelity in juveniles. In contrast, 18 of the 121 cross-cohort HS pairs identified were captured between the two closest river systems (c. 150 km apart) demonstrating recent male breeding movements between these rivers, but not more widely. Mitogenomic analyses revealed river specific long-term female reproductive philopatry. Allele frequency differences in the nuclear SNP data were observed between the river systems. However, between the two closest river systems, this only reflected the restricted movements of juveniles since it was not evident when FS and HS pairs were discarded. Accounting for juvenile river fidelity, female philopatry and the presence of two distinct gene pools is important for the management of this threatened species.