CRISPR-associated DinG protein (CasDinG) is essential to type IV-A CRISPR function. However, the enzymatic activities of CasDinG are unknown. Here we demonstrate that CasDinG from Pseudomonas aeruginosa strain 83 is an ATP- and metal-dependent 5′-3′ DNA helicase. The crystal structure of CasDinG reveals a helicase core of two RecA-like domains with three accessory domains (N terminal, arch, and vestigial FeS). To examine the in vivo function of these CasDinG domains, we first identified the preferred PAM sequence (5′-GNAWN-3′ on the 5′-side of the target) with a plasmid library containing all combinations of the five nucleotides upstream of the target sequence. Plasmid clearance assays (using a 5′-GGAAA-3′ PAM) with CasDinG domain mutants demonstrated the vFeS and arch accessory domains are both essential for type IV immunity. These results provide a needed structural and biochemical framework for understanding the type IV-A CRISPR system.