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The Beijing genotype is the most distributed <i>M. tuberculosis</i> family in Kazakhstan. In this study, we identified dominant Beijing clusters in Kazakhstan and assessed their drug susceptibility profiles and association with the most widely spread mutation Ser531Leu of the <i>rpoB</i> gene and the mutation Ser315Thr of the <i>katG</i> gene associated with resistance to rifampicin and isoniazid, respectively. <i>M. tuberculosis</i> isolates (<i>n</i> = 540) from new TB cases were included in the study. MIRU-VNTR genotyping was performed for 540 clinical isolates to determine <i>M. tuberculosis</i> families using 24 loci. RD analysis was additionally performed for the Beijing isolates. The identification of mutations in the drug-resistance genes of <i>M. tuberculosis</i> was performed with allele-specific real-time PCR and Sanger sequencing. The Beijing genotype was identified in 60% (324/540) of the clinical isolates. Central Asian/Russian cluster 94-32 was the most distributed cluster among the Beijing isolates (50.3%; 163/324). Three other dominant Beijing clusters were identified as 94-33 (3.4%; 11/324), 100-32 (3.1%; 10/324) and 99-32 (3.1%; 10/324). The Beijing genotype was associated with drug-resistant TB <i>(p</i> < 0.0001), including multidrug-resistant TB <i>(p</i> < 0.0001), in our study. An association of the mutation Ser531Leu of the <i>rpoB</i> gene with the Beijing genotype was found (<i>p</i> < 0.0001; OR = 16.0000; 95%CI: 4.9161–52.0740). Among the Beijing isolates, cluster 94-32 showed an association with MDR-TB (<i>p</i> = 0.021). This is why the evaluation of the Beijing genotype and its clusters is needed to control MDR-TB in Kazakhstan.