The horizontal gene transfer facilitated by mobile genetic elements impacts almost all areas of bacterial evolution, including the accretion and dissemination of antimicrobial-resistance genes in the human and animal pathogen Staphylococcus aureus. S. aureus strains frequently harbour diverse plasmids conferring multiple antimicrobial resistances, however, bioinformatic genome surveys of staphylococcal plasmids have revealed an unexpected paucity of conjugation and mobilisation loci, which has led some to assume that conjugative plasmid transfer plays only a minor role in the evolution of this genus. Here we review historically documented staphylococcal conjugative plasmids and highlight that at least three distinct and widely distributed families of conjugative plasmids currently contribute to the dissemination of antimicrobial resistance in Staphylococcus. We also discuss our recently discovered "relaxase-in trans" mechanisms of conjugative mobilisation facilitated by conjugative plasmids pWBG749 and pSK41, and explain how this mechanism may facilitate the horizontal transmission of around 90% of plasmids that were previously considered non-mobilisable. Finally, we enumerate unique sequenced S. aureus plasmids with potential mechanism of mobilisation and predict that at least 80% of all non-conjugative S. aureus plasmids are mobilisable by at least one mechanism. We suggest that a greater research focus on the molecular biology of conjugation is essential if we are to recognise gene-transfer mechanisms from our increasingly in silico analyses.