Polyploidization events are observed across the tree of life and occurred in many fungi, plant and animal species. Polyploidy is thought to be an important source of speciation and tumorigenesis. However, the origins of polyploid populations are not always clear and little is known about the precise nature and structure of their complex genome. Using a long-read sequencing strategy, we sequenced a large number of isolates from the Brettanomyces bruxellensis yeast species, which is found in anthropized environments (e.g. beer, contaminant of wine, kombucha and ethanol production) and characterized by several polyploid subpopulations. To reconstruct the polyploid genomes, we phased them by using different strategies and we found that each subpopulation had a unique polyploidization history with distinct trajectories. The polyploid genomes contain either genetically closely related (with a genetic divergence < 1%) or diverged copies (> 3%), indicating auto- as well as allopolyploidization events. These latest events have occurred independently with a specific and unique donor in each of the polyploid subpopulations, and exclude the known Brettanomyces sister species as possible donors. Finally, loss of heterozygosity events have shaped the structure of these polyploid genomes and underline their dynamic. Overall, our study highlights the multiplicity of the trajectories leading to polyploid genomes within a same species.