Pathogens secrete effector molecules that facilitate the infection of their hosts. A number of effectors identified in plant pathogenic Phytophthora species possess N-terminal motifs (RXLR-dEER) required for targeting these effectors into host cells. Here, we bioinformatically identify >370 candidate effector genes in each of the genomes of P. sojae and P. ramorum. A single superfamily, termed avirulence homolog (Avh) genes, accounts for most of the effectors. The Avh proteins show extensive sequence divergence but are all related and likely evolved from a common ancestor by rapid duplication and divergence. More than half of the Avh proteins contain conserved C-terminal motifs (termed W, Y, and L) that are usually arranged as a module that can be repeated up to eight times. The Avh genes belong to the most rapidly evolving part of the genome, and they are nearly always located at synteny breakpoints. The superfamily includes all experimentally identified oomycete effector and avirulence genes, and its rapid pace of evolution is consistent with a role for Avh proteins in interaction with plant hosts.