The dairy production system is a cornerstone of the agri-food chain, delivering vital nutrition and simultaneously serving as a major reservoir for antibiotic-resistant bacteria. Given the mounting global concern over antibiotic resistance, it is crucial to gain knowledge on the prevalence of antibiotic-resistant bacteria within the organized dairy production system. In this study, 48 samples of milk, faeces, soil, and wastewater were collected from four distinct dairy farms. An antibiotic-guided approach was used for the isolation of putative antibiotic-resistant bacteria, utilizing three different growth media and eight antibiotics, categorized as critical and high priority by the World Health Organization. A total of 615 putative antibiotic-resistant bacteria were successfully isolated, and 393 of these isolates were identified using 16S rRNA gene sequencing and MALDI-TOF techniques. The majority of the bacterial isolates belonged to the phylum Pseudomonadota (59%), followed by Bacillota (12%), Bacteroidota (8%), and Actinomycetota (3%). A total of 51 different genera, encompassing 125 distinct species, were identified. Among them, the most predominant genera was Escherichia (22%, 85), followed by Pseudomonas (11%, 42) and Acinetobacter (9%, 34). Among the identified putative antibiotic resistant bacteria, 274 were closely related to critical-, high-, medium- and healthcare-associated pathogens. A total of 153 falling into these different categories were successfully analyzed for their antibiotic resistance potential. It was found that beta lactam resistance was prevalent in dairy production systems, with extended spectrum cephalosporin-resistant Escherichia coli being predominant. Furthermore, this study found more than 20 multi-drug-resistant bacteria (13%) belonging to critical-, high-, medium- and healthcare-associated pathogens in the dairy production system. In conclusion, this study emphasizes the necessity for effective management strategies to combat the challenge of antibiotic-resistant bacteria in the dairy production system.