Protein-resolved multi-omic mapping defines a comparative virus–host atlas for LayV, NiV and HeV, integrating interactomes, matched transcriptomes, quantitative proteomes and structural models across 26 viral proteins. Henipa-related viral proteins retain substantial interaction specificity, yet converge on shared host regulatory programs, revealing host-node convergence as a conserved organizing principle across divergent paramyxoviruses. Matrix proteins emerge as conserved host-engagement hubs that connect henipa-related viruses to two host-control axes: ABT1-linked transcriptional regulation and MRPS35-linked mitochondrial ribosome function. M–MRPS35 engagement is conserved across multiple henipa-related viruses and is associated with progressive mitochondrial ultrastructural damage, membrane-potential collapse and loss of cellular fitness. ABT1 chromatin profiling reveals that M proteins redirect a basal transcription-associated regulator toward altered antiviral and immune-related transcriptional pro