Harbouring a plasmid often imposes a fitness cost on the bacterial host. Motivated by implications for public health, the majority of studies on plasmid cost are focused on elements that impart antibiotic resistance. Plasmids, however, can provide a wide range of ecologically important phenotypes to their bacterial hosts-such as virulence, specialized catabolism and metal resistance. The Agrobacterium tumefaciens tumour-inducing (Ti) plasmid confers both the ability to infect dicotyledonous plants and to catabolize the metabolites that plants produce as a result of being infected. We demonstrate that this virulence and catabolic plasmid imposes a measurable fitness cost on host cells under resource-limiting, but not resource replete, environmental conditions. Additionally, we show that the expression of Ti-plasmid-borne pathogenesis genes necessary to initiate cooperative pathogenesis is extremely costly to the host cell. The benefits of agrobacterial pathogenesis stem from the catabolism of public goods produced by infected host plants. Thus, the virulence-plasmid-dependent costs we demonstrate constitute costs of cooperation typically associated with the ability to garner the benefits of cooperation. Interestingly, genotypes that harbour derived opine catabolic plasmids minimize this trade-off, and are thus able to freeload upon the pathogenesis initiated by other individuals.