Biological invasions have significant ecological, evolutionary and economic consequences. Ants are exemplary invaders and their invasion success is frequently attributed to a shift in social structure between native and introduced populations. Here, we use a multidisciplinary approach to determine the social structure, origin and expansion of the invasive Argentine ant, Linepithema humile, in Australia by linking behavioural and genetic studies with indicators of dispersal pathways and propagule pressure. Behavioural assays revealed a complete absence of aggression within and between three cities – Melbourne, Adelaide and Perth – spanning 2700 km across Australia. Microsatellite analyses showed intracity genetic homogeneity and limited but significant intercity genetic differentiation. Exceptions were two Perth nests that likely represent independent translocations from Adelaide. These patterns suggest efficient local gene flow with more limited jump dispersal via transport corridors between cities. Microsatellite analyses of L. humile from potential source regions, combined with data from port interceptions, trade pathways and the timeline of spread within Australia, implicate the main European supercolony as the source of L. humile in Melbourne. Such an introduction probably then redistributed across Australia and spread to New Zealand to form an expansive Australasian supercolony.