Small crustaceans populate nearly every aquatic ecosystem, often representing the most diverse and abundant component of metazoan communities. These taxa comprise a rich lexicon of unexplored viral diversity. Circular replication initiator protein-encoding ssDNA (CRESS-DNA) viruses are cosmopolitan members of microcrustacean viral consortia. Despite their prevalence among invertebrates, the paradigms that govern CRESS-DNA virus phylogenomics, biogeography, and ecology in arthropods are largely unknown. This dissertation couples viromic sequencing, viral surveillance, and metazoan transcriptomics to examine novel ssDNA virus genotypes, infer the influence of metazoan phylogenetics on viral distribution, and assess the relationship between these viruses and the biology of putative invertebrate hosts. Viromes from microcrustacean populations from disparate aquatic habitats were sequenced to compare CRESS-DNA virus genomes on a multi-ecosystem scale, enabling identification of 215 putatively novel and microdiverse genotypes. Identification of endogenized viral elements established a paleovirological record of historical arthropod-virus interactions. Pairwise sequence comparison indicated that novel CRESS-DNA viruses shared similarity with genotypes recovered from similar microcrustaceans. Several genotypes – specifically those associated with benthic amphipods of genus Diporeia – were further explored to resolve the role of microcrustacean speciation on CRESS-DNA virus biogeography and determine the potential influence of viral load on microcrustacean ecology. Among three identified viral genotypes associated with Diporeia spp., one (LM29173) was both prevalent and recurrent among amphipod populations in the Laurentian Great Lakes. Occurrence of this genotype coincided with amphipod haplotype demographics, indicating the potential for host specificity. Transcriptomes from both amphipod haplotype were compared, with load of LM29173 corresponding with significant over- or under-expression of >2,000 de novo assembled amphipod transcripts, though no change in microcrustacean nutritional quality was detected. Collectively, these studies demonstrate the diversity of CRESS-DNA viruses among microcrustaceans and address fundamental questions about their ecogenomics in non-model arthropod systems.