The asexual ectomycorrhizal fungus Cenococcum geophilum has a wide geographic range in diverse forest ecosystems. Although its genetic diversity has been documented at a stand or regional scale, knowledge of spatial genetic structure is limited. We studied the genetic diversity and spatial structure of C. geophilum in eight Japanese coastal pine forests with a maximum geographic range of 1364 km. A total of 225 samples were subjected to phylogenetic analysis based on the glyceraldehyde 3-phosphate dehydrogenase gene (GAPDH) followed by microsatellite analysis with five loci. The phylogenetic analysis based on GAPDH resolved three groups with most isolates falling into one dominant lineage. Microsatellite analyses generated 104 multilocus genotypes in the overall populations. We detected significant genetic variation within populations and genetic clusters indicating that high genetic diversity may be maintained by possible recombination processes at a stand scale. Although no spatial autocorrelation was detected at a stand scale, the relationship between genetic and geographic distances among the populations was significant, suggesting a pattern of isolation by distance. These results indicate that cryptic recombination events at a local scale and unknown migration events at both stand and regional scales influence spatial distribution and genetic structure of C. geophilum in coastal pine forests of Japan.