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The emerging tick-borne pathogen Anaplasma phagocytophilum infects humans, domestic animals, and wildlife throughout the Holarctic. In the western US, the ecology of A. phagocytophilum is particularly complex, with multiple pathogen strains, tick vectors, and reservoir hosts. A recent phylogenetic analysis of A. phagocytophilum strains isolated from various small mammal hosts in California documented distinct clustering of woodrat strains separate from sciurid (chipmunk and squirrel) strains. Here, we identified strains of A. phagocytophilum in various Ixodes tick species in California and related these genotypes to those found among reservoir and clinical hosts from the same areas. The sequences from all of the nidicolous (nest-dwelling) Ixodes ticks grouped within a clade that also contained all of the woodrat-origin A. phagocytophilum strains. Two of the I. pacificus sequences were also grouped within this woodrat clade, while the remaining five belonged to a less genetically diverse clade that included several sciurid-origin strains as well as a dog, a horse, and a human strain. By comparing A. phagocytophilum strains from multiple sources concurrently, we were able to gain a clearer picture of how A. phagocytophilum strains in the western US are partitioned, which hosts and vectors are most likely to be infected with a particular strain, and which tick species and reservoir hosts pose the greatest health risk to humans and domestic animals.