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Honey bees provide essential pollination services to the terrestrial ecosystem and produce important agricultural products. As a beneficial lactic acid bacterium, <i>Enterococcus faecium</i> is often supplied as a probiotic for honey bees and other animals. However, the underlying mechanisms of its actions and possible safety risks are not well understood. We present the first complete genome sequence of <i>E. faecium</i> isolated from the honey bee gut using nanopore sequencing, and investigate the effects and mechanisms of interactions between <i>E. faecium</i> and honey bees via transcriptome and miRNA analysis. <i>E. faecium</i> colonization increased honey bee gut weight. Transcriptome analysis showed that developmental genes were up-regulated. In accordance, the target genes of the down-regulated miRNAs were enriched in developmental pathways. We describe how <i>E. faecium</i> increases honey bee gut weight at the transcriptional and post-transcriptional levels, and add insights about how miRNAs mediate host and bacteria interactions.