Recent studies have found that three divergent lineages of the ectomycorrhizal fungus Cenococcum geophilum may co-occur within a single soil sample. To test how inference of population structure is affected by species concept, potential recombination in this putative asexual fungus was analyzed by sequencing 10 loci from 44 isolates from within one main lineage that is potentially sub-divisible into two phylogenetic species (A and B). Phylogenetic incongruence between these loci and recombination analyses using six different methods was consistent with recombination. However, most of the incongruence was caused by an apparently reciprocal recombination event between the actin locus and the other loci studied. Extreme divergence between the two types of actin loci suggests either an ancient recombination event or a more recent horizontal inheritance. We also found that random mating could not be rejected when A and B isolates were treated as members of a single species based on multilocus disequilibrium analyses, whereas random mating was rejected when all isolates were pooled. These results are significant and demonstrate that inferences of population structure can be confounded when isolates are pooled together based entirely on a morphological species concept.