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Systematic study in the genus <i>Alternaria</i> provides a unique opportunity to examine speciation processes across different fungal lifestyles and microbial ecology. The genus encompasses nearly 200 species, but most fall into two very distinct sister clades: Section Alternata, which represents wide-spread facultative pathogens, and Section Porri, which represents host-specific facultative sabrobes. Twelve species from each Section have been sequenced using Illumina Next Generation Sequencing technology and functionally annotated based on gene prediction in one reference genome for each Section: <i>A. arborescens</i> for Section Alternata and <i>A. solani</i> for Section Porri. Whole genome comparisons revealed orthologs in high synteny within groups rather than between, supporting Section designation. Homology was much lower among host-specific species within Section Porri than among nonhost-specific species within Section Alternata, suggesting ancestral barriers to genetic exchange by host despite common sympatric associations. Gene ontology analysis also revealed differential enrichment in certain functional categories, suggesting that each Section encompasses some distinct metabolic pathways. Genomic polymorphisms revealed most species are clearly delimited by host within Section Porri, but indicated genetic exchange among clusters of species within Section Alternata, which may support their collapse into fewer taxonomic units.<p><p>Keywords: