Viral non-coding RNAs (ncRNAs) often perform multiple functions during persistent infection, but how they interface with host RNA-binding proteins remains incompletely understood. Herpesvirus saimiri (HVS), a T-tropic γ-herpesvirus that induces aggressive lymphomas in primates, during its latency expresses abundant small nuclear RNAs HSUR1 and HSUR2. HSUR1 is known to trigger target-directed microRNA decay (TDMD) of host miR-27a, and HSUR2 can function as a miRNA-dependent adaptor; here we show that both HSURs also bind host Pumilio proteins (PUM1 and PUM2) via perfectly conserved Pumilio response elements (PREs). PUM proteins are potent post-transcriptional regulators that bind PREs usually located in 3' UTRs of mRNAs to repress protein production. In Jurkat T cells, wild-type HSUR1/2, but not PRE-mutant variants, shift cells from a naïve-like toward an effector/memory-like state. This PRE-dependent shift is evidenced by increased surface expression of CXCR3, a chemokine receptor of activated effector T cells, and CD57, a marker of terminally differentiated T and NK cells. Our data support a model in which HSURs sequester a fraction of PUM proteins. Consistently, depletion of PUM1 or PUM2 phenocopies HSUR-induced changes, with more abundant PUM1 exerting the dominant effect. Consistently, depletion of PUM1 or PUM2 phenocopies HSUR-induced changes, with more abundant PUM1 exerting the dominant effect. In BJAB B cells, HSUR1 still drives PRE-dependent gene regulation, but the affected genes only partially overlap with those in Jurkat cells, and some transcripts even show reversed direction of change, revealing strong cell-type specificity. By identifying PUM1/2 as key host partners of HSUR ncRNAs, this work uncovers an underappreciated role for PUM proteins in shaping T- and B-cell states and reveals an additional way in which γ -herpesviral ncRNAs reprogram lymphocytes to promote viral persistence.