Atomic models of unbound Csy complex (PDB ID: 6B45), Csy bound to a partially duplexed dsDNA (PDB ID: 6B44), and Csy bound to a complete dsDNA target (PDB ID: 6MPU) were used to generate a dynamic model of the conformational changes undergone during DNA binding. The Csy complex initially engages DNA through non-sequence-specific electrostatic interactions, followed by sequence-specific interactions with the protospacer adjacent motif (PAM). Incoming DNA is immobilized in a vice formed by the N-terminal domain of the large subunit (Cas8f) and the opposing face of the terminal backbone subunit (Cas7f.6). Residues in Cas8f detect the PAM in the minor groove, locally distorting the DNA duplex and facilitating strand invasion. The complementary DNA strand hybridizes with the crRNA guide, forming an R-loop that is stabilized by positively-charged residues in an “R-loop binding channel” that terminates near the 3’ end of the crRNA spacer. Formation of the complete R-loop is critical for rotation of the C-terminal helical bundle of Cas8f and recruitment of the trans-acting nuclease-helicase Cas2/3. A virally-encoded anti-CRISPR protein (AcrIF3) is a molecular mimic of the Cas8f helical bundle, and comparison of the two structures reveals a “nuclease recruitment helix” on Cas8f that is exposed by the ~180° rotation of the helical bundle. Collectively, the model explains how the Csy complex coordinates nuclease recruitment to bona fide dsDNA targets.