The factors that determine the extent to which diffusion and thermal activation processes govern electron transfer (ET) between proteins are debated. The process of ET between plastocyanin (PC) and cytochrome f (CytF) from the cyanobacterium Phormidium laminosum was initially thought to be diffusion-controlled but later was found to be under activation control (Schlarb-Ridley, B. G.; et al. Biochemistry 2005, 44, 6232). Here we describe Brownian dynamics simulations of the diffusional association of PC and CytF, from which ET rates were computed using a detailed model of ET events that was applied to all of the generated protein configurations. The proteins were modeled as rigid bodies represented in atomic detail. In addition to electrostatic forces, which were modeled as in our previous simulations of protein-protein association, the proteins interacted by a nonpolar desolvation (hydrophobic) force whose derivation is described here. The simulations yielded close to realistic residence times of transient protein-protein encounter complexes of up to tens of microseconds. The activation barrier for individual ET events derived from the simulations was positive. Whereas the electrostatic interactions between P. laminosum PC and CytF are weak, simulations for a second cyanobacterial PC-CytF pair, that from Nostoc sp. PCC 7119, revealed ET rates influenced by stronger electrostatic interactions. In both cases, the simulations imply significant contributions to ET from both diffusion and thermal activation processes.