The Polyomaviridae family contains members known for achieving high seroprevalence within their target species despite a limited genomic economy. Minimalism, by definition, allows for the clarification and streamlining of purpose via the removal of unnecessary or distracting components. Among viruses, Simian Vacuolating Virus 40 (SV40) and other polyomaviruses are master minimalists, achieving efficient replication and persistence with compact genomes of approximately 5 kb in length. This review examines how polyomaviruses employ limited genetic material and simple structure to participate in complex functions and interactions, highlighting minimalism as both an evolutionary and functional advantage. Polyomaviruses make the most of their compact genomes in each stage of the viral lifecycle through the production of multifunctional early proteins and cis-regulatory elements, utilization of alternative splicing and host infrastructure, and organization of compact structural proteins. This allows for the successful replication and proliferation of virions while also reducing evolutionary pressure and promoting host immune evasion. Examination of the implications of polyomaviral minimalism illustrates that genome economy is not a constraint, but rather a driver of biological sophistication.