AbstractMultiple introductions are key features for the establishment and persistence of introduced species. However, little is known about the contribution of genetic admixture to the invasive potential of populations. To address this issue, we studied the recent invasion of the Asian tiger mosquito (Aedes albopictus) in Europe. Combining genome‐wide single nucleotide polymorphisms and historical knowledge using an approximate Bayesian computation framework, we reconstruct the colonization routes and establish the demographic dynamics of invasion. The colonization of Europe involved at least three independent introductions in Albania, North Italy and Central Italy that subsequently acted as dispersal centres throughout Europe. We show that the topology of human transportation networks shaped demographic histories with North Italy and Central Italy being the main dispersal centres in Europe. Introduction modalities conditioned the levels of genetic diversity in invading populations, and genetically diverse and admixed populations promoted more secondary introductions and have spread farther than single‐source invasions. This genomic study provides further crucial insights into a general understanding of the role of genetic diversity promoted by modern trade in driving biological invasions.