Deltaviruses are subviral agents of animals, which, in humans, require a hepadnavirus helper for transmission. The absence of deltavirus-like endogenous viral elements (δEVEs) has prevented an understanding of their evolution in deep time. By screening the representative genomes of all metazoans for endogenous delta antigen-like sequences, we report the discovery of 13 δEVEs in the genomes of five species of termites. Analysis of 906 transcriptomes reveals widespread expression of δEVEs across termite taxa, including a co-opted δEVE-nucleoplasmin fusion gene with an exon/intron structure. We also describe seven exogenous termite deltaviruses found in diverse tissues and castes. The absence of a hepadnavirus in deltavirus-positive samples indicates that termite deltaviruses may use alternative virus helpers or different mechanisms for transmission within a colony. Our analyses reveal that deltaviruses have stably coexisted with termites since their origin (∼141 million years ago [mya]) and implicate at least one cross-phylum transmission event between the termite and vertebrate lineages.