Virus diseases are causing high yield losses in crops worldwide. The Barley yellow dwarf virus (BYDV) complex is responsible for one of the most widespread and economically important viral diseases of cereals. While no complete resistance gene has been uncovered in the primary genepool of barley, sources of resistance were identified in the wild relative Hordeum bulbosum, representing the secondary genepool of barley. One such locus, Ryd4Hb, has been previously introgressed into barley, and was allocated to chromosome 3H, but is tightly linked to a sublethality factor that prevents the incorporation and utilization of Ryd4Hb in barley varieties. To solve this problem, we fine-mapped Ryd4Hb and separated it from this negative factor. We narrowed the Ryd4Hb locus to a 66.5 kbp physical interval in the barley 'Morex' reference genome. The region comprises one complete and one partial gene from the nucleotide-binding and leucine-rich repeat immune receptor family, typical of dominant virus resistance genes. The closest homolog to these two Ryd4Hb candidate genes is the wheat Sr35 stem rust resistance gene. In addition to the fine mapping, we reduced the sublethality factor interval to 600 kbp in barley. Aphid feeding experiments demonstrated that Ryd4Hb provides a direct resistance to BYDV rather than a resistance to its vector. The presented results, including the high-throughput molecular markers, will permit a more targeted selection of the resistance in breeding, enabling the use of Ryd4Hb in barley varieties.