Double-stranded DNA viruses including bacteriophage and herpesviruses package their genomes into empty capsids during viral replication, using an ATP-driven motor. The capsid expands to accommodate the full genome and maintain viable DNA densities. Structural and functional studies of the mechanism of DNA packaging and capsid expansion are required to understand the molecular basis of these processes, and how these steps are coordinated. To advance such research, this study focused on bacterial virus P23-45, which infects thermophilic bacterium Thermus thermophilus. It is shown that empty capsids can be packaged with DNA in vitro in the presence of the packaging ATPase. Both the unexpanded procapsid and expanded capsid were packaged when ATP was provided. Optimal packaging was observed at 50–65 ◦C, consistent with the system’s thermophilic origin. Expanded capsids were more active at packaging DNA than procapsids. Cryo-electron microscopy reconstructions determined at 3.7 Å and 4.4 Å resolution for the expanded capsid and procapsid respectively, revealed capsids had T=7 laevo quasi-symmetry. Capsids possessed a “supersized” capsid lattice spacing of ~17 nm, ~20 % larger than the 13–14 nm spacing observed in other bacteriophage and herpesviruses. Consequently, P23-45 capsids are larger and can accommodate twice the expected length of DNA for a capsid of this protein fold and symmetry. This is demonstrative of an additional evolutionary strategy available to viruses in modifying capsid size. The unique vertex of the icosahedral capsids containing the portal protein was characterised in both capsids, revealing a spacious interface between the 5-fold symmetrical vertex and the 12-fold portal protein. Parallel studies on the evolutionarily related encapsulin compartment from Myxococcus xanthus revealed a decameric oligomer of ferritin-like protein EncB is responsible for mineralisation of iron in the encapsulin core. These cores are likely similar in composition and structure to those of ferritin.