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Abstract Mobile genetic elements (MGEs), such as plasmids and bacteriophages, are major contributors to the ecology and evolution of host-associated microbes due to a continuum of symbiotic interactions and by mediating gene flow via horizontal gene transmission. However, while myriad studies have investigated relationships between MGEs and variation in fitness among microbial and eukaryotic hosts, few studies have incorporated this variation into the context of MGE evolution and ecology. Combining HiC-resolved metagenomics with the model honey bee worker gut microbiome, we show that the worker gut contains a dense, nested MGE community that exhibits a wide degree of host range variation among microbial hosts. Using measures of gene similarity and syntenty, we show that plasmids likely mediate gene flow between individual honey bee colonies, though these plasmids exhibit broad host range variation within their individual microbiomes. We further show that phage-microbe networks exhibit high variation among individual metagenomes, and that phages show broad host range with respect to both the number and phylogenetic distance of their hosts. Finally, we provide evidence that measures of nucleotide variation positively correlate with host range in bee-associated phages, and that functional targets of diversifying selection are partitioning differently between broad or narrow host range phages. Our work underscores the variability of MGE x microbial interactions within host-associated microbial communities and highlights the genomic variation associated with MGE host range diversity.