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• Nation-wide genomic analysis could detect seven different phases of SARS-CoV-2 pandemic in India. • Variant of concern and variant of interest were dominated only post-first wave in India. • More than 0.5 million mutational events could be detected across 20,086 high quality genomes. • Four major mutational events i.e., spike (D614G), NSP 12b (P314L), NSP3 F106F and 5′ UTR 241 occurring in more than 19,000 genomes. COVID-19 has posed unforeseen circumstances and throttled major economies worldwide. India has witnessed two waves affecting around 31 million people representing 16% of the cases globally. To date, the epidemic waves have not been comprehensively investigated to understand pandemic progress in India. Here, we aim for pan Indian cross-sectional evolutionary analysis since inception of SARS-CoV-2. High quality genomes, along with their collection date till 26th July 2021, were downloaded. Whole genome-based phylogeny was obtained. Further, the mutational analysis was performed using SARS-CoV-2 first reported from Wuhan (NC_045512.2) as reference. Based on reported cases and mutation rates, we could divide the Indian epidemic into seven phases. The average mutation rate for the pre-first wave was <11, which elevated to 17 in the first wave and doubled in the second wave (∼34). In accordance with mutation rate, VOCs and VOIs started appearing in the first wave (1.5%), which dominated the second (∼96%) and post-second wave (100%). Nation-wide mutational analysis depicted >0.5 million mutation events with four major mutations in >19,300 genomes, including two mutations in coding (spike (D614G), and NSP 12b (P314L) of rdrp), one silent mutation (NSP3 F106F) and one extragenic mutation (5′ UTR 241). Whole genome-based phylogeny could demarcate post-first wave isolates from previous ones by point of diversification leading to incidences of VOCs and VOIs in India. Such analysis is crucial in the timely management of pandemic. [ABSTRACT FROM AUTHOR]