Sporothrix species (Ascomycota, Ophiostomatales) are dimorphic fungi with diverse ecological niches, ranging from mammalian, plant, and insect pathogens to fungicolous organisms. Here, we describe Sporothrix davidellisii (CBS 147636T), a novel pathogenic species within the S. pallida complex isolated from a case of feline sporotrichosis in Melbourne, Australia. Phylogenetic analyses based on ITS, β-tubulin (BT2), calmodulin (CAL), and translation elongation factor 1-α (EF1-α) sequences confirmed its distinctiveness, with ITS sequence identity to its closest relative (S. chilensis) not exceeding 97.6%. The assembled genome is 39.02 Mb (eight contigs) with a 27.2 kb mitochondrial genome and a total of 12,631 predicted genes. Genetic diversity analyses revealed moderate nucleotide variation in the ITS region (π = 0.055), greater diversity in BT2 (π = 0.098), and CAL (π = 0.118), supporting its status as a unique species. Morphological studies revealed distinctive characteristics differentiating S. davidellisii from its nearest relatives, including elongated clavate sympodial conidia and sessile conidia. Notably, S. davidellisii exhibits yeast-like growth at 37°C, forming ellipsoid to ovoid budding cells in liquid media, although cigar-shaped yeasts, characteristic of highly virulent Sporothrix species, are rarely observed. This ability to transition to a yeast-like form, combined with its high-temperature tolerance (growth up to 40°C), underscores its opportunistic pathogenic potential. The pathogenic role of S. davidellisii highlights the importance of monitoring atypical Sporothrix infections in feline hosts, which may serve as environmental sentinels for emerging fungal pathogens. These findings expand the taxonomy of Sporothrix, contributing to our understanding of the evolutionary complexity and zoonotic potential of species within the S. pallida complex.