Despite theoretical expectations, marine microeukaryote population are often highly structured and the mechanisms behind such patterns remain to be elucidated. These organisms display huge census population sizes, yet genotyping usually requires clonal strains originating from single cells, hindering proper population sampling. Estimating allelic frequency directly from population wide samples, without any isolation step, offers an interesting alternative. Here, we validate the use of meta-transcriptome environmental samples to determine the population genetic structure of the dinoflagellate Alexandrium minutum. Strain and meta-transcriptome based results both indicated a strong genetic structure for A. minutum in Western Europe, to the level expected between cryptic species. The presence of numerous private alleles, and even fixed polymorphism, would indicate ancient divergence and absence of gene flow between populations. Single nucleotide polymorphisms (SNPs) displaying strong allele frequency differences were distributed throughout the genome, which might indicate pervasive selection from standing genetic variation (soft selective sweeps). However, a few genomic regions displayed extremely low diversity that could result from the fixation of adaptive de novo mutations (hard selective sweeps) within the populations.