Poultry enteric bacterial diseases are of significant economic importance because they are responsible for production losses due to weight loss, increased morbidity and mortality, and increased cost of production arising from poor feed conversion and treatment. This cross-sectional purposive study characterized enteric bacterial pathogens in poultry from selected agroclimatic regions in Kenya and investigated their antimicrobial resistance gene profiles. Cloacal (n = 563) and oropharyngeal (n = 394) swabs were collected and pooled into 16 and 14 samples, respectively, to characterize bacterial pathogens and their antimicrobial resistance gene profiles. We report that Proteobacteria, Chlamydiae, and Firmicutes are the most dominant phyla present in both cloacal and oropharyngeal swabs of the six poultry species studied, indicating the colonization of the poultry gut by many pathogenic bacteria. Using KEGG and COG databases, some pathways related to metabolism, genetic information, and cellular processing were detected. We also report the abundance of antimicrobial resistance genes that confer resistance to β-lactamases, aminoglycosides, and tetracycline in most of the poultry analyzed, raising concern about the dangers associated with continuous and inappropriate use of these antibiotics in poultry production. The antimicrobial resistance gene data generated in this study provides a valuable indicator of the use of antimicrobials in poultry in Kenya. The information generated is essential for managing bacterial diseases, especially in backyard poultry raised under scavenging conditions.