The microsporidian Vairimorpha (Nosema) ceranae is one of the most common parasites of the honeybee. A single honeybee carries many parasites and therefore multiple alleles of V. ceranae genes that seem to be ubiquitous. As a consequence, nucleotide diversity analyses have not allowed discriminating genetic structure of parasite populations. We performed deep loci-targeted sequencing to monitor the haplotype frequencies of genome markers in isolates from discontinuous territories, namely the tropical islands of the South West Indian Ocean. The haplotype frequency distribution corroborated the suspected tetraploidy of the parasite. Most major haplotypes were ubiquitous in the area but with variable frequency. While oceanic isolates differed from European and Asian outgroups, parasite populations from distinct archipelagoes also differed in their haplotype distribution. Interestingly an original and very divergent Malagasy isolate was detected. The observed population structure allowed formulating hypotheses upon the natural history of V. ceranae in this oceanic area. We also discussed the usefulness of allelic distribution assessment, using multiple informative loci or genome-wide analyses, when parasite population is not clonal within a single host.