Rabbit haemorrhagic disease virus (RHDV) is a highly virulent calicivirus that infects and frequently kills rabbits. The RNA-dependent RNA polymerase (RdRp) of RHDV and related lagoviruses accumulate in distinct, as yet uncharacterised subcellular structures and induce a redistribution of Golgi membranes. Here, we report on a partially hidden hydrophobic motif that determines the subcellular localisation of recombinant RHDV RdRps in transfected rabbit kidney (RK-13) cells. This motif, 189LLWGCDVGVAVCAAAVFHNICY210, is located within the F homomorph of the RdRp core. Analysing recombinant RdRps with or without the hydrophobic motif suggests that it is critical for the subcellular localisation of the RdRp. Furthermore, fusing the motif to GFP kept the resulting fusion protein in the cytoplasm, in contrast to the native GFP protein. Moreover, amino acid substitutions that decrease the hydrophobicity of the motif reduced the ability of RdRp variants to accumulate at multiple subcellular foci and to induce changes to the Golgi network. However, the RdRp protein structure suggests that the hydrophobic motif is largely buried, which should preclude membrane interactions. Molecular dynamics simulations revealed that neighbouring structural elements are highly labile and could give way upon an association with membrane surfaces. Interestingly, three collinear lysines on the surface of the RdRp may not only attract the protein to negatively charged membrane surfaces, but could also position it such that the emerging hydrophobic motif would face the membrane and immerse itself into the outer leaflet. Our findings contribute to a better understanding of the molecular virulence mechanism of a virus that is highly pathogenic but cannot be grown in culture.