Human‐facilitated introductions of nonnative populations can lead to secondary contact between allopatric lineages, resulting in lineage homogenisation or the formation of stable hybrid zones maintained by reproductive barriers. We investigated patterns of gene flow between the native Sacramento Valley red fox (Vulpes vulpes patwin) and introduced conspecifics of captive‐bred origin in California's Central Valley. Considering their recent divergence (20–70 kya), we hypothesised that any observed barriers to gene flow were primarily driven by pre‐zygotic (e.g. behavioural differences) rather than post‐zygotic (e.g. reduced hybrid fitness) barriers. We also explored whether nonnative genes could confer higher fitness in the human‐dominated landscape resulting in selective introgression into the native population. Genetic analysis of red foxes (n = 682) at both mitochondrial (cytochrome b + D‐loop) and nuclear (19,051 SNPs) loci revealed narrower cline widths than expected under a simulated model of unrestricted gene flow, consistent with the existence of reproductive barriers. We identified several loci with reduced introgression that were previously linked to behavioural divergence in captive‐bred and domestic canids, supporting pre‐zygotic, yet possibly hereditary, barriers as a mechanism driving the narrowness and stability of the hybrid zone. Several loci with elevated gene flow from the nonnative into the native population were linked to genes associated with domestication and adaptation to human‐dominated landscapes. This study contributes to our understanding of hybridisation dynamics in vertebrates, particularly in the context of species introductions and landscape changes, underscoring the importance of considering how multiple mechanisms may be maintaining lineages at the species and subspecies level.