Species of the phylum Blastocladiomycota, early-diverging zoosporic (flagellated) lineages of fungi, are vastly understudied. This phylum includes the genus , which consists of more than 80 fungal species that are obligate parasites of arthropods. Known species lack a complete asexual life cycle, instead surviving through an obligate heterecious alternation of generations life cycle. Despite their global distribution and interesting life cycle, little is known about the genomics of any species. To address this, we generated three draft-level genomes and annotations for representing its haploid meiospore, orange gamete, and amber gamete life stages. These draft genome assemblies ranged in size from 5002 to 5799 contigs, with a total length of 19.8-22.8 Mb and a mean of 7416 protein-coding genes. We then demonstrated the utility of these genomes by combining the draft annotations as a reference for analysis of transcriptomes. We analyzed transcriptomes from across host-associated life stages, including infected larvae and excised mature sporangia from the mosquito . We identified differentially expressed genes and enriched GO terms both across and within life stages and used these to make hypotheses about biology. Generally, we found the transcriptome to be a complex and dynamic expression landscape; GO terms related to metabolism and transport processes were enriched during infection and terms related to dispersal were enriched during sporulation. We further identified five high mobility group (HMG)-box genes in , three belonging to clades with mating type (MAT) loci from other fungi, as well as four ortholog expansions in compared with other fungi. The genomes and transcriptomes reported here are a valuable resource and may be leveraged toward furthering understanding of the biology of these and other early-diverging fungal lineages.