Natural killer (NK) cells are innate lymphocytes that exhibit features of adaptive immunity, including antigen-specific clonal expansion and long-lived memory, which play a critical role in antiviral responses such as those against cytomegalovirus (CMV). Although NK cell expansion has been attributed to cytokine-regulated transcriptional networks, here we identify a cytokine-independent mechanism mediated by canonical WNT signaling. In this study, we found that NK cells uniquely express the WNT ligand receptor Frizzled-5 (Fzd5), which is essential for regulating β-catenin-dependent canonical WNT signaling. Using mouse CMV (MCMV) infection as a model to study antigen-specific NK cell responses, we demonstrate that the WNT-Fzd5 signaling pathway requires β-catenin as a co-factor and LEF1 as a downstream transcription factor to activate key regulators of cell cycle entry and proliferation. These findings establish Fzd5-mediated canonical WNT signaling and LEF1 activity as critical drivers of the adaptive NK cell response during viral infection, offering new insights into the regulation of innate immunity.