Coronavirus Disease 2019 (COVID-19) warrants comprehensive investigations of publicly available Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) genomes to gain new insight about their epidemiology, mutations, and pathogenesis. Nearly 0.4 million mutations have been identified so far among the ∼60,000 SARS-CoV-2 genomic sequences. In this study, we compared a total of 371 SARS-CoV-2 published whole genomes reported from different parts of Bangladesh with 467 sequences reported globally to understand the origin of viruses, possible patterns of mutations, and availability of unique mutations. Phylogenetic analyses indicated that SARS-CoV-2 viruses might have transmitted through infected travelers from European countries, and the GR clade was found as predominant in Bangladesh. Our analyses revealed 4604 mutations at the RNA level including 2862 missense mutations, 1192 synonymous mutations, 25 insertions and deletions and 525 other types of mutation. In line with the global trend, D614G mutation in spike glycoprotein was predominantly high (98 %) in Bangladeshi isolates. Interestingly, we found the average number of mutations in ORF1ab, S, ORF3a, M, and N were significantly higher (p < 0.001) for sequences containing the G614 variant compared to those having D614. Previously reported frequent mutations, such as R203K, D614G, G204R, P4715L and I300F at protein levels were also prevalent in Bangladeshi isolates. Additionally, 34 unique amino acid changes were revealed and categorized as originating from different cities. These analyses may increase our understanding of variations in SARS-CoV-2 virus genomes, circulating in Bangladesh and elsewhere.