Identifying mechanisms that underpin animal migration patterns and examining variability in space use within populations is crucial for understanding population dynamics and management implications. In this study, we quantified the migration rates, seasonal changes in migratory connectivity, and residency across population demographics (age and sex) to understand the proximate cues of migration timing in American horseshoe crabs (Limulus polyphemus). Juvenile (n = 25) and adult (n = 70) horseshoe crabs were tracked with acoustic telemetry techniques for a 3-yr period in Moriches Bay, NY. Connectivity metrics and residency probability were quantified through spatial network analysis and empirically derived Markov Chain models (EDMC), respectively. The migratory probability of adult horseshoe crabs between Moriches Bay and the Atlantic Ocean was estimated to be 41.0% (95% CI: 34.0–59.8); in contrast, only 8% (95% CI: 1.2–31.6) of juveniles migrated into the ocean. Migration timing was influenced by the interaction of photoperiod and temperature, revealing seasonal differences in migration timing and a 50% narrower range of photoperiod and temperature over which fall migrations occurred compared to spring. Sex-specific differences in space use and connectivity within each season were largely absent; however, centralized habitats were important for maintaining connectivity across all seasons. EDMC results revealed that when standardized to the number of horseshoe crab detections on each receiver, the centrally located habitats in Moriches Bay and Inlet accounted for >50% of the total relative residency probability within most seasons, indicating these areas may be preferred by adult horseshoe crabs. Ontogenetic differences in maximum spatial extent, space use, and connectivity were observed in the bay, as juveniles exhibited lower linkages between locations (n = 4) relative to adults (n = 13) during the same temporal period. Our work highlights the application of novel quantitative approaches for addressing the movement dynamics of horseshoe crabs that can be readily applied to other taxa in the context of wildlife conservation.