Copepoda is the most abundant taxon in deep‐sea hydrothermal vents, where hard substrate is available. Despite the increasing interest in seafloor massive sulphides exploitation, there have been no population genomic studies conducted on vent meiofauna, which are known to contribute over 50% to metazoan biodiversity at vents. To bridge this knowledge gap, restriction‐site‐associated DNA sequencing, specifically 2b‐RADseq, was used to retrieve thousands of genome‐wide single‐nucleotide polymorphisms (SNPs) from abundant populations of the vent‐obligate copepod Stygiopontius lauensis from the Lau Basin. SNPs were used to investigate population structure, demographic histories and genotype–environment associations at a basin scale. Genetic analyses also helped to evaluate the suitability of tailored larval dispersal models and the parameterization of life‐history traits that better fit the population patterns observed in the genomic dataset for the target organism. Highly structured populations were observed on both spatial and temporal scales, with divergence of populations between the north, mid, and south of the basin estimated to have occurred after the creation of the major transform fault dividing the Australian and the Niuafo'ou tectonic plate (350 kya), with relatively recent secondary contact events (<20 kya). Larval dispersal models were able to predict the high levels of structure and the highly asymmetric northward low‐level gene flow observed in the genomic data. These results differ from most studies conducted on megafauna in the region, elucidating the need to incorporate smaller size when considering site prospecting for deep‐sea exploitation of seafloor massive sulphides, and the creation of area‐based management tools to protect areas at risk of local extinction, should mining occur.