Understanding the genomic and ultimate eco-evolutionary factors underlying the diversification of fungal organisms is a major goal for evolutionary mycologists, and a key step towards comparative eukaryotic speciation genetics. Access to whole-genome sequences and advanced computational methods provide mycologists with powerful tools to disentangle the complex evolutionary history of fungi. Speciation genomics approaches based on the application of population genomic models at the intra- inter-specific boundary are changing our view of the factors and mechanisms underlying fungal diversification, revealing that processes such as introgression, hybridization, rapid speciation, and horizontal gene transfer had been overlooked. The filamentous fungus Neurospora is an emerging model to study fungal speciation. Neurospora discreta PS4, in particular, has a very large distribution and is therefore an ideal system to investigate the eco-evolutionary drivers and genomic correlates of fungal diversification. Previous studies have shown deep population structure within N. discreta PS4 with limited admixture, but the structure of the species at finer scale, and the extent of admixture and gene flow between lineages remains unclear. Here, we used re-sequencing of 128 isolates representing 17 sites in Europe, North America and Asia to infer the evolutionary history of N. discreta PS4. We confirmed the existence of five lineages; one in Papua New Guinea, one in Thailand and three in USA and Europe, and found a new lineage distributed in both Portugal and Washington (USA). Our analyses reveal deep divergence between lineages, with virtually no admixture. Most sampled sites harbored only a single lineage of N. discreta PS4 but at least five sites harbored two or three lineages coexisting in sympatry without evidence for genetic mixing. We discuss the factors that may have contributed to the divergence of lineages, their co-occurrence in sympatry, and their maintenance without admix