Archaeal viruses are well known for their diverse morphologies and extreme stability. Here, we used cryo–electron tomography to analyze the structure of Sulfolobus ellipsoid virus 1 (SEV1), an archaeal virus with an ellipsoidal shape and a lipid envelope, and its infection strategy. We show that the SEV1 nucleocapsid adopts a “coil-stacking” architecture with substantial flexibility. The major capsid protein VP4, whose homologs are widespread in the thermoacidic environments around the Pacific Rim, binds genomic DNA in the formation of a nucleoprotein filament with a “beads-on-a-string” appearance. The virion is notably stable at high temperature and acidic pH, and the envelope of SEV1 is crucial to the thermostability of the virion. The infected cell undergoes cytoplasmic condensation to form patches associated with the assembly intermediates of the progeny virions. The nascent virions are released through virus-associated pyramids (VAPs), which are constructed of an SEV1 protein distinctly different at the amino acid sequence level from other known VAP proteins.