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Characterizing the molecular interactions of viruses in natural microbial populations offers insights into virus–host dynamics in complex ecosystems. We identify the resistance ofSulfolobus islandicustoSulfolobusspindle‐shaped virus (SSV9) conferred by chromosomal deletions of pilin genes,pilA1andpilA2that are individually able to complement resistance. Mutants with deletions of bothpilA1andpilA2or the prepilin peptidase, PibD, show the reduction in the number of pilins observed in TEM and reduced surface adherence but still adsorb SSV9. The proteinaceous outer S‐layer proteins, SlaA and SlaB, are not required for adsorption nor infection demonstrating that the S‐layer is not the primary receptor for SSV9 surface binding. Strains lacking both pilins are resistant to a broad panel of SSVs as well as a panel of unrelatedS. islandicusrod‐shaped viruses (SIRVs). Unlike SSV9, we show thatpilA1orpilA2is required for SIRV8 adsorption. In sequencedSulfolobusstrains from around the globe, one copy of eachpilA1andpilA2is maintained and show codon‐level diversification, demonstrating their importance in nature. By characterizing the molecular interactions at the initiation of infection betweenS. islandicusand two different types of viruses we hope to increase the understanding of virus–host interactions in the archaeal domain.