Cryptosporidium species cause cryptosporidiosis, characterized by acute gastroenteritis in humans and animals worldwide. Knowledge of the diversity of Cryptosporidium among mammals and birds is incomplete, especially in North American passerines. In this first molecular study of Cryptosporidium in a North American passerine, C. parvum and a novel genotype, called the red-winged black bird genotype were isolated. Genetic characteristics and phylogenetic analyses of the red-winged black bird genotype were described at the 18S rRNA, actin and HSP70 loci, and it was distinct from previously described species and genotypes. The novelty of this genotype was also supported by propagation studies in chickens, zebra finches and cockatiels that failed to produce patent infections. The study adds to our understanding of the co-evolution of the parasite with its hosts and potential sources of C. parvum transmission to susceptible human and animal hosts.