Research on the genetics of invasive species often focuses on patterns of genetic diversity and population structure within the introduced range. However, a growing body of literature is demonstrating the need to study the native range, and how native genotypes affect both ecological and evolutionary mechanisms within the introduced range. Here we used genotyping‐by‐sequencing to study both native and introduced ranges [based on 1,653 single nucleotide polymorphisms (SNPs)] of the amphiatlantic marine invertebrate Ciona intestinalis. A previous study using microsatellites analysed samples collected along the Swedish west coast and showed the presence of genetically distinct lineages in deep and shallow waters. Using our SNP data from newly collected samples (285 individuals), we first confirmed the presence of this depth‐defined genomic divergence along the Swedish coast. We then used Approximate Bayesian Computation to infer the historical relationship among sites from the North Sea, the English Channel and the northwest Atlantic and found evidence of ancestral divergence between individuals from deep waters off Sweden and individuals from the English Channel. This divergence was followed by a secondary contact that led to a genetic admixture between the ancestral populations (i.e. deep Sweden and English Channel), which originated the genotypes found in shallow Sweden. We then revealed that the colonisation of C. intestinalis in the northwest Atlantic was as a result of an admixture between shallow Sweden and the English Channel genotypes across the introduced range. Our results showed the presence of both past and recent genetic admixture events that together may have promoted the successful colonisations of C. intestinalis. Our study suggests that secondary contacts potentially reshape the evolutionary trajectories of invasive species through the promotion of intraspecific hybridisation and by altering both colonisation patterns and their ecological effects in the introduced range.