Viruses are the most abundant and diverse organisms on Earth, though only a small portion cause disease. Understanding viral diversity is key to understanding and predicting pathogen emergence and zoonotic spillover. Here, we use meta-transcriptomic sequencing to examine the viral communities in the ileum of 25 Northern Mockingbirds (Mimus polyglottos) from various locations across Texas. We assembled high-quality genomes of 43 viral species (40 species identified to 13 families, one to kingdom, and two to realm), 38 of which were novel. They tentatively represent avian- (n = 3), arthropod- (n = 21), plant- (n = 5) and fungi- (n = 4) associated, or other (n = 10) viruses. The arthropod-associated Dicistroviridae family was the most dominant, comprising known and potentially new species. Of potential epidemiological importance were three novel and avian-associated viruses: members of the families Hepeviridae and Picornaviridae, and a new Matryoshka RNA virus. The Matryoshka RNA virus 8 (MaRNAV-8) is sister to other Matryoshka RNA viruses, and its co-occurrence with haemosporida further supports the nested virus-parasite-vector-vertebrate host relationship of this group of viruses, with potential implications for parasite evolution, fitness and load and vector competence. The Picornaviridae virus is a member of an avian hepatovirus clade, found nested within a clade containing both the mammalian pathogens Hepatovirus A – I and the avian Tremovirus pathogens, suggestive of a newly discovered pathogen of Northern Mockingbird. Although the recovered Hepeviridae virus is of unknown pathology, its family members include the Hepatitis E viruses. With the great diversity and novelty described from ileal viromes, discriminating potential pathogens and commensal microbiota from viruses associated with food items remains challenging. A deeper understanding of virus transmission and the risk of potential zoonosis can be enhanced by tracking viruses through the food web and via inter-specific and predator-prey interactions, particular in areas subject to land-use change, where human-wildlife interactions are increased and the risks from emerging pathogens of veterinary and medical importance are more pronounced.