The HSV endoribonuclease VHS is a key viral factor that induces the global degradation of host cell mRNAs, thereby evading antiviral responses and promoting virus translation while suppressing host translation. VHS is thought to associate with the host translation initiation machinery and cleave associated mRNAs which are then degraded by the host 5’-3’ exoribonuclease XRN1. While several protein-protein interactions have been implicated in this process, the precise RNA sequences targeted by VHS remain unclear. We have adopted a process known as hyperTRIBE to reveal for the first time precisely where VHS interacts with the host transcriptome. VHS was fused to the hyperactive, catalytic domain (cd) of the RNA-editing enzyme ADAR, which induces A-to-I modifications in surrounding nucleotides. This resulted in a fusion protein that retained full VHS activity, indicating that ADAR(cd) did not interfere with VHS-RNA interactions. To map VHS association with RNA, a well-characterised catalytically inactive mutant of VHS was then fused to ADAR(cd) to produce a fusion protein that can associate stably with RNA without cleaving it, allowing the ADAR(cd) to induce stable modifications in surrounding nucleotides and mark the VHS association sites. This approach has precisely mapped the VHS footprint to the first 120 nucleotides of a reporter transcript where two A-to-I modifications were found, 32 nucleotides apart. Extending this data, RNA-sequencing of the modified host transcriptome has now provided the first high-resolution map of VHS-RNA interactions in human cells. This study establishes hyperTRIBE as a versatile platform for mapping viral RNA-binding proteins.