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Abstract: The genomes of RNA-viruses are dynamic and adopt certain structures to facilitate replication, translation and evade cellular immunity while inside their host cell cytoplasm. However, a lack of methodology has limited our knowledge to the structure of encapsidated genomes inside mature virus particles or in-vitro folded viral RNAs, hence uncoupled from infection. Here we present a genome-wide method for probing RNA base-pairing during viral infection, and utilize it to study the genomic structure of Zika virus inside human cells. We reveal multiple structural motifs along the virus genome and provide a physical evidence for a cyclic structure the virus RNA adopts during replication. We highlight unforeseen base-pairing between the Zika genome and human small non-coding RNAs. Our methodology opens up opportunities for characterization of pathogenic RNA genomes while propagating inside their host and offers a platform for development of new RNA-based therapeutic strategies.