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Communities of symbiotic microbes obtained from the environment are an integral component of animal fitness and ecology. Thus a general and practical understanding of the processes that drive microbiome assembly and structure are paramount to understanding animal ecology, health, and evolution. We conceptualized a series of ecological filters that operate at the environment, host, and host tissue levels during microbiome assembly and discuss key ecological processes that structure animal microbiomes at each level. We conducted a survey of crayfish across four sites within the contiguous range of the of stream-inhabiting crayfish Cambarus sciotensis in western Virginia, USA, to characterize multiscale variation in the crayfish microbiome. We also conducted an in situ experiment to assess local drivers of microbial diversity on the closely related Cambarus chasmodactylus. We used a combination of DNA fingerprinting and next-generation sequencing to characterize microbiome diversity and composition from crayfish carapaces and gills to identify key filters affecting microbiome structure. Field survey showed that local environment and host tissues interact to create patterns of microbial diversity and composition, but the strongest effects on microbial community structure were observed at the level of host tissue. Our field experiment confirmed strong effects of host tissue, and also showed that a metazoan ectosymbiont which feeds on biofilms (Annelida; Branchiobdellida) had significant effects on microbial composition of the host carapace. Crayfish carapaces were colonized by diverse and taxonomically even microbial communities that were similar to, and correlated with, microbial communities of the ambient environment. Conversely, crayfish gills were colonized by less diverse communities and dominated by two families of bacteria with potentially significant functional roles: Comamonadaceae and Chitinophagaceae. Our results suggest that microbial assembly of the carapace is driven by external biotic and abiotic processes, whereas assembly on the gills appears to be coupled to host biology that favors interactions with few specific taxa. Our work shows how multi-scale studies of symbiont community assembly provide valuable insights into how the animal microbiome is structured under conditions of natural complexity and help identify other symbiont taxa, i.e., the branchiobdellidans, that may further influence microbiome assembly and structure.