The side group of the amino acid arginine is typically in its guanidinium protonated form under physiological conditions and participates in a broad range of ligand binding and charge transfer processes of proteins. The recognition of phosphate moieties by guanidinium plays a particularly key role in the interactions of proteins with ATP and nucleic acids. Moreover, it has been recently identified as the driving force for the inhibition of kinase phosphorilation activity by guanidinium derivatives devised as potential anticancer agents. We report on a fundamental investigation of the interactions and coordination arrangements formed by guanidinium with phosphoric, phosphate, and pyrophosphate groups. Action vibrational spectroscopy and ab initio quantum chemical computations are employed to characterize the conformations of benchmark positively charged complexes isolated in an ion trap. The multidentate structure of guanidinium and of the phosphate groups gives rise to a rich conformational landscape with a particular relevance of tweezer-like configurations, where phosphate is effectively trapped by two guanidinium cations. The pyrophosphate complex incorporates a Na+ cation, which serves to compare the interactions associated with the localized versus diffuse charge distributions of the alkali cation and guanidinium, respectively, within a common supramolecular framework.