Homologous recombination (HR) is a high-fidelity pathway for repairing DNA double-strand breaks (DSBs) that is choreographed by the HR machinery, the DNA-damage checkpoint, and cell-cycle regulators. A central challenge in HR is locating a homologous DNA template while maintaining genome integrity. The transient intermediates that arise during homology search are dynamically regulated by multiple factors, ultimately shaping repair outcomes. Two key DNA motors in this process are Rad54 and Rdh54, Snf2-family ATP-dependent DNA translocases that remodel the Rad51-mediated presynaptic complex to promote template location and strand invasion. However, how these motors are regulated and how they function mechanically during homology search remain open questions.Here, I show that phosphorylation of Rdh54 by the effector kinase Rad53 decouples ATP hydrolysis from DNA translocation, thereby increasing HR fidelity. Structural modeling suggests that the phosphorylation site lies at an intermolecular interface, consistent with regulation through protein-protein interactions. I also identify a separation-of-function mutant of Rad54 that exhibits reduced motor activity due to an increased DNA dissociation rate. Within the presynaptic complex, the mutant regains approximately 60% of wildtype translocation activity but remains less capable of resisting external forces. In vivo, the mutant suppresses the Rad51-overexpression phenotype and is synthetically lethal with srs2∆, indicating that a later pathway rather than presynaptic filament assembly is primarily affected. The mutant displays reduced efficiency in D-loop capture and DNA repair in ectopic recombination, but its repair deficiency in allelic recombination can be compensated by longer-track gene conversion events. This suggests that the HR intermediates formed by the mutant are less stable but can be functionally rescued by extended homology. The instability of these intermediates also leads to increased frequencies of non-crossover (NCO) and reinvasion-induced break-induced replication (BIR) events. Taken together, I propose a DNA compaction model, in which Rad54 locally compacts large fragments of DNA through multiple Rad54-DNA contacts, enabling a 1-dimensional search within the constrained DNA. A stable anchor motor is critical for maintaining this structure and ensuring efficient search. The separation-of-function Rad54 mutant loses the ability to clamp and constrain DNA, rendering search intermediates more vulnerable to mechanical disruption and thereby reducing homology search efficiency.