Community health workers play a critical role as intermediaries between communities and public health systems, for delivering key maternal and child health and nutrition interventions in low and middle-income countries. Female frontline health workers (FEHWs) led India’s COVID-19 response in 2020. A capabilities approach emphasising on their digital and health literacy helped unpack systemic inequalities that women suffer, inequalities in resources and opportunities, educational deprivations, the failure of work to be recognized as work, and insults to bodily integrity. We studied FFHWs’ role in sub national and local health response to the COVID-19 pandemic in six states in India—Odisha, Bihar, Madhya Pradesh, Uttaralchand, Kerala and Maharashtra – using interviews and policy analysis. The data was thematically analysed, and studied within the government policies and guidelines to combat the emerging concerns in COVID-19. It is essential to recognise FFHWs’ role inside the health system, improving their working conditions and enabling enhanced usage of information, communication and technology. Concerted efforts by policy-makers are required to recalibrate how FFHWs are empowered as leaders of change with systems-level change and impetus through recognition and rewards. This alone will address issues of parity, equity, participation, and representation in a gender-responsive health system.