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<i>Histoplasma capsulatum</i> is a dimorphic fungus associated with respiratory and systemic infections in mammalian hosts that have inhaled infective mycelial propagules. A phylogenetic reconstruction of this pathogen, using partial sequences of <i>arf</i>, <i>H-anti</i>, <i>ole1</i>, and <i>tub1</i> protein-coding genes, proposed that <i>H. capsulatum</i> has at least 11 phylogenetic species, highlighting a clade (BAC1) comprising three <i>H. capsulatum</i> isolates from infected bats captured in Mexico. Here, relationships for each individual locus and the concatenated coding regions of these genes were inferred using parsimony, maximum likelihood, and Bayesian inference methods. Coalescent-based analyses, a concatenated sequence-types (CSTs) network, and nucleotide diversities were also evaluated. The results suggest that six <i>H. capsulatum</i> isolates from the migratory bat <i>Tadarida brasiliensis</i> together with one isolate from a <i>Mormoops megalophylla</i> bat support a NAm 3 clade, replacing the formerly reported BAC1 clade. In addition, three <i>H. capsulatum</i> isolates from <i>T. brasiliensis</i> were classified as lineages. The concatenated sequence analyses and the CSTs network validate these findings, suggesting that NAm 3 is related to the North American class 2 clade and that both clades could share a recent common ancestor. Our results provide original information on the geographic distribution, genetic diversity, and host specificity of <i>H. capsulatum</i>.