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Identifying the origins and colonization routes of alien species is critical to understanding the mechanisms, consequences and management of invasions. This study aims to demonstrate and explain conflicting genetic signals in a widespread invasive Ponto-Caspian mysid Paramysis lacustris using mitochondrial DNA and microsatellite markers. Native Black Sea populations of P. lacustris are divided into three distinct phylogeographic groups: Danube–Dniester region, coastal Danube lakes, and Dnieper River delta. In the 1950s–1970s the species has been extensively used for relatively well documented transplantations in Eastern Europe. However, the populations in the newly established distribution area do not match any of the known native groups, and their genetic signal does not correspond with the recorded transplantation history. Using Bayesian Approximate Computation we explore alternative scenarios that could explain the unexpected mitochondrial and nuclear signals in the introduced populations. We suggest that reservoir construction and break-up of natural dispersal barriers on the River Dnieper have brought about a novel stock, probably admixed from a previously isolated and unknown “relict” population in the middle Dnieper and the genetically distinct Dnieper delta lineage. Through further intentional transfers this new P. lacustris lineage is now widely present in Eastern Europe and is likely to have new gene and trait combinations. The conflicting mitochondrial-nuclear signal in non-native populations also highlights the importance of using multiple genetic markers when tracing invasion sources and pathways.