Risk of beef contaminated by E. coli O157:H7 is affected by prevalence of O157:H7 in cattle feces. Host genetics may influence O157:H7 shedding and overall microbial diversity in the lower gastrointestinal tract. Objectives of this study were to determine influence of animal genotypes on measures of O157:H7 shedding and relative abundance of different taxa in cattle feces, and identify regions of the bovine genome associated with O157:H7 prevalence and microbial diversity. Feces were sampled from fall born animals (n = 1,099) of various breed composition (crosses of 18 different breeds) undergoing trials to measure individual animal intake over 63 to 90 d periods. Steers (n = 574) received a high-energy finishing ration and heifers (n = 525) a high-roughage breeding development diet. Feces were sampled once before, at least thrice during, and once after the feed intake trial period. Individual samples were assessed for enumerable O157:H7. Taxonomic composition of the fecal microbiome was quantified from shotgun metagenome sequencing of total DNA pooled for each animal. Reads were assembled for each animal individually and contigs pooled within and across animals by phylogeny, yielding a reference metagenome assembly of 87 different taxonomic groups that were detected across > 75% of the animals. These taxa were quantified by mapping reads from each sample onto the reference assembly. Heritability for relative abundance of each taxa and O157:H7 prevalence measure was estimated with REML, using genomic relationships described by imputed BovineHD SNP genotypes. Individual SNP effects were solved from animal solutions after REML converged. Heritability estimates ranged from 0.00 for 35 taxa to 0.21 for Butyrivibrio, and were greater than 0.05 for 19 taxa. For O157:H7 traits, estimates were 0.10 for the number of times the animal was prevalence positive, and 0.07 for log₁₀ of the average O157:H7 level. Correlations between SNP effects on O157:H7 and individual taxa were near zero, although a cluster of SNP between TMEM20 and PLCE1 on BTA26 was associated with log₁₀[0157:H7] and 11 taxa having heritabilities >0.05.