Cryptosporidium is a genus of ubiquitous parasites that have been detected worldwide in nearly 500 species of amphibians, birds, fish, mammals, and reptiles. Most research has focused on the Cryptosporidium species and genotypes infecting humans and livestock, because of the public health significance and economic importance of the diarrheal disease cryptosporidiosis. Relatively little is known about Cryptosporidium-host dynamics in wildlife hosts, even though a wide range of wildlife species are susceptible to Cryptosporidium. Insights into ecology and host-parasite dynamics in wild populations are necessary to understand the biology and evolution of Cryptosporidium; to predict the emergence of human and livestock pathogens; and to clarify Cryptosporidium taxonomy and systematics. The focus of this research was to study the ecology of Cryptosporidium in populations of cricetid (voles, Peromyscus mice, muskrats) and sciurid (squirrels and chipmunks) rodents, and characterize Cryptosporidium taxa by sequencing multiple genetic loci (18S rRNA and actin genes). Paralogous copies of the 18S rRNA gene in Cryptosporidium genotypes from wild rodents were common and affected phylogenetic inferences. Eastern chipmunks (Tamias striatus) were infected with Cryptosporidium chipmunk genotype II, which had 18S rRNA gene paralogs that shared ~93% similarity. The degree of divergence has not been previously described in any Cryptosporidium taxa, but is similar to the divergence described in Plasmodium species, which have functionally distinct 18S rRNA gene copies. Marmotini squirrels were mainly host to novel Cryptosporidium genotypes, and to the best of our knowledge, we provide the first molecular characterization of Cryptosporidium in black-tailed prairie dogs (Cynomys ludovicianus). Cryptosporidium host adaptation and specificity was not evident in in Sciurini rodents and they were host to two zoonotic taxa, C. ubiquitum and Cryptosporidium skunk genotype. In conclusion, Cryptosporidium was prevalent in cricetid and sciurid rodents, and the extent of host adaptation varied among Cryptosporidium taxa as they are likely shaped by differences in host-parasite ecology and evolution. The rodents sampled are not significant reservoirs of zoonotic Cryptosporidium, with the exception of tree squirrels. Sequencing multiple genetic loci helped identify the presence of paralogs and resolve cryptic Cryptosporidium taxa, which strengthened phylogenetic inferences leading to a better understanding of Cryptosporidium systematics.