Even during the current COVID‐19 crisis, venture capital (VC) is booming in India. Indian‐based VC funds grew from less than 10 at the start of the 1990s to more than 500 nowadays, with the amount of total investment continuously increasing since 2000. The aim of this paper is to contextualize the process of emergence, development, and boom of the Indian VC industry from the theoretical perspective of innovation and entrepreneurial systems, particularly incorporating contributions from Latin American and Indian authors. In doing so, we present a global, historical, and territorially grounded narrative of the Indian VC development stressing the relevance of: (a) the institutional and technological capabilities accumulated by the Indian National Innovation System (NIS) and the Indian Computer and Information Services Entrepreneurial Ecosystem (CISEE), particularly around Bangalore, (b) the role of the State (and the institutional entrepreneurs) and the timing of the STI policy oriented to the software industry, (c) the growing influence of global players such as the World Bank, the Indian American argonauts and multinational enterprises, and (d) the U.S. offshoring opportunities and the growing Indian domestic demand. We discuss these processes with a wider relevance for theoretical and policy advancement in Global South settings.