Plasmids are major drivers of microbial evolution, enabling horizontal gene transfer and facilitating adaptation through the dissemination of relevant genes and traits. Little is known about plasmid diversity and function in extremophiles. \'Fervidacidithiobacillus caldus\' a meso-thermo-acidophilic sulfur oxidizer, is a key player in sulfur cycling in acidic environments. Here, we present a comprehensive analysis of the plasmidome, and associated anti-mobile genetic element defense systems, across genomes of this species and metagenomes from diverse natural and industrial settings harboring \'F. caldus\'. We identified >30 distinct plasmids, representing five consistent replication-mobilization families. Plasmids ranged in size between 2.5-65 kb, with gene content and plasmid modularity scaling with element size and copy numbers inversely correlating with size. Plasmids carried variable numbers of hypothetical proteins and transposases, with annotated cargo genes reflecting functional differentiation by habitat. Defensome profiling revealed over 50 anti-MGE systems in sequenced \'F. caldus\' isolates, including diverse innate and adaptive systems. In environmental populations, an inverse relationship was observed between defensome complexity and plasmidome abundance and diversity, underscoring a pivotal role of the host defensome in modulating persistence, compatibility, and overall plasmid diversity across \'F. caldus\' populations. Yet, other plasmids appeared decoupled from both host abundance and defensome complexity, suggesting potential host shifts, environmental persistence, or differential replication under suboptimal growth conditions for the host. Altogether, these findings reveal a modular, adaptive plasmidome shaped by selective pressures and host-plasmid-defensome interactions, and positions plasmids as key contributors to adaptation, gene flow, and functional innovation in this extreme acidophile.