While higher education is crucial for the development of ideals and skills necessary for democratic societies to take root and prosper, higher education institutions’ missions have been tested during this time of uncertainty. The Covid-19 pandemic has revealed the instabilities and disparities in global higher education by exacerbating profound social fractures and long-standing structural imbalances. As such, the study examined how the Covid-19 pandemic has affected rural higher education institutions in building a sustainable and democratic future. It also examined students and staffs’ perspectives on how these higher education institutions responded to the Covid-19 pandemic in building a resilient, inclusive and democratic culture. Informed by an interpretivist paradigm, the study utilised a qualitative research approach and a case study design. Data were collected at two rural universities from university managers, lecturers and students using interviews. The study’s findings revealed that while the Covid-19 pandemic represents a time of survival of the fittest, which also strengthened democratic tenets and revolutionised the higher education sector, the pandemic has revealed pre-existing institutional issues and vulnerabilities in rural higher education institutions. Research findings also revealed that the pandemic has also spotlighted the poor and the most vulnerable in society as rural HEIs endeavoured to build resilience, and an inclusive and democratic culture to stay sturdy in the face of the ‘new normal’ and emerge stronger from the Covid-19 pandemic. Based on the study’s findings, it was concluded that building a resilient, inclusive and democratic culture at HEIs could generate success for higher education institutions by influencing students’ career opportunities and employment readiness, amongst many others. We recommend that HEIs consider focusing more on equity and inclusion; reinforce capacities for risk management at all levels of the system; strong leadership and coordination; and enhance consultation and communication mechanisms.