Early-life microbial exposures profoundly impact individuals’ lifelong health trajectories by shaping immune maturation and modulating disease risk, e.g. as typified by the “hygiene hypothesis.” Childcare facilities represent a critical yet understudied source of microbial exposures where preschool-aged children spend 7-10 hours daily during key developmental periods. This study presents the first multi-omic and multi-kingdom investigation of microbial transmission and community ecology across childcare environments, integrating microbiome samples from both high-touch and low-touch surfaces with children’s nasal and oral microbiomes, using full-length amplicon sequencing (16S and ITS) paired with short-read and long-read metagenomic sequencing. Our findings revealed distinct microbial signatures across these environments, with human-associated microorganisms predominating in high-touch areas, while greater taxonomic diversity characterizes low-touch areas. Specifically, on high touch surfaces, several bacterial and fungal species were shared between host and environmental communities, such as food-associated Lactococcus lactis and Streptococcus thermophilus, suggesting defined transmission routes via host shedding, environmental exposures, and food consumption. With improved genomic resolution and reconstruction from paired short- and long-read metagenomics, we identified novel lateral gene transfer (LGT) events enriched for mobile elements, DNA-interacting domains, and adaptive elements such as antibiotic resistance and virulence factors. These methods also shed light on viral ecology, such as Caudoviricetes bacteriophages ubiquitous across host and environmental communities with phylogenetically-differentiated niche- and bacterial host-specific lineages. The positive relationship between the host prediction frequency and its community relative abundance suggested host abundance (availability)-driven phage-bacteria population dynamics. This work highlights previously understudied components of early-life microbial exposures in childcare environments with enhanced resolution, and it provides methods for identifying potential pathogen reservoirs, tracking transmission routes, and developing targeted interventions.