Two new structures of the SRP GTPase, Ffh, have been determined at 1.1Å resolution, and provide the basis for comparative examination of the extensive water structure of the apo conformation of these GTPases. We identify a set of well-defined water-binding positions in the active site of the two-domain 'NG' GTPase, as well as at two functionally important interfaces. The water hydrogen bonding network accommodates alternate conformations of the protein sidechains by undergoing local rearrangements, and, in one case, illustrates binding of a solute molecule within the active site by displacement of water molecules without further disruption of the water interaction network. A subset of the water positions are well defined in several lower resolution structures, including those of different nucleotide binding states; these appear to function in maintaining the protein structure. Consistent arrangements of surface water between three different ultra-high resolution structures provide a framework for beginning to understand how local water structure contributes to protein-ligand and protein-protein binding in the SRP GTPases.