Marssonina coronaria Ellis & Davis is a filamentous fungus in the class Leotiomycetes that causes apple blotch, an economically important disease of apples worldwide. Here, we sequenced the whole genome of M. coronaria strain NL1. The genome contained 50.3 Mb with 589 scaffolds and 9,622 protein-coding genes. A phylogenetic analysis using multiple loci and a whole-genome alignment revealed that M. coronaria is closely related to Marssonina rosae and Marssonina brunnea. A comparison of the three genomes revealed 90 species-specific carbohydrate-active enzymes, 19 of which showed atypical distributions, and 12 species-specific secondary metabolite biosynthetic gene clusters, two of which have the potential to synthesize products analogous to PR toxin and swainsonine, respectively. We identified 796 genes encoding for small secreted proteins in Marssonina spp., many encoding for unknown hypothetical proteins. In addition, we revealed the genetic architecture of the MAT1-1 and MAT1-2 mating-type loci of M. coronaria, as well as 16 tested isolates carrying either MAT1-1 idiomorph (3) or MAT1-2 idiomorph (13). Our results showed a series of species-specific carbohydrate-active enzyme, secondary metabolite biosynthetic gene clusters and small-secreted proteins that may be involved in the adaptation of Marssonina spp. to their distinct hosts. We also confirmed that M. coronaria possesses a heterothallic mating system and has outcrossing potential in nature.