P-element induced wimpy testis (PIWI) interacting RNA (piRNA) are essential for fertility, by protecting the integrity of the germ-line genome via silencing of transposable elements (TE). Because new TE are constantly invading the host genome, piRNA-producing loci are under continuous pressure to undergo rapid evolution. This arms race between TE and piRNA is a prime example of the genome being more plastic than previously thought. Historically, the study of piRNA and TE has benefited from the use of diverse model organisms, including worms, fruit fly, zebrafish, frogs, and mice. In domestic chickens, we recently identified a new mode of piRNA acquisition in which the host hijacks and converts a pre-existing provirus into a piRNA-producing locus to defend against Avian leukosis virus, an adaptive immune strategy similar to the prokaryotic CRISPR–Cas [clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated (Cas)] system. This finding reveals a previously unrecognized mechanism of the host piRNA repertoire to rapidly evolve and target TE specifically. In this review, we will focus on both the unique and common features of chicken piRNA, as well as the advantages of using chickens as a model system, to address fundamental questions regarding piRNA acquisition in hosts. We will also comment on the potential application of piRNA for improving poultry health and reproductive efficiency.