Human-aided transport is responsible for many contemporary species introductions, yet the contribution of human-aided transport to dispersal within non-native regions is less clear. Understanding dispersal dynamics for invasive species can streamline mitigation efforts by targeting routes that contribute disproportionally to spread. Because of its limited natural dispersal ability, rapid spread of the Asian tiger mosquito (Aedes albopictus) has been attributed to human-aided transport, but until now the relative roles of human-aided and natural movement have not been rigorously evaluated. Here, we use landscape genetics and information-theoretic model selection to evaluate 52 models representing 9,240 pair-wise dispersal paths among sites across the US range for Ae. albopictus, and show that recent gene flow reflects a combination of natural and human-aided dispersal. Highways and water availability facilitate dispersal at a broad spatial scale, but gene flow is hindered by forests at the current distributional limit (range-edge) and by agriculture among sites within the mosquito's native climatic niche (range-core). Our results show that highways are important to genetic structure between range-edge and range-core pairs, suggesting a role for human-aided mosquito transport to the range edge. In contrast, natural dispersal is dominant at smaller spatial scales, reflecting a shifting dominance to natural movement two decades after introduction. These conclusions highlight the importance of: (a) early intervention for species introductions, particularly those with readily dispersed dormant stages and short generation times, and (b) strict monitoring of commercial shipments for transported immature stages of Ae. albopictus, particularly towards the northern edge of the US range.