A fundamental problem in genome biology is to elucidate the evolutionary forces responsible for generating nonrandom patterns of genome organization. As the first metazoan to benefit from full-genome sequencing, Caenorhabditis elegans has been at the forefront of research in this area. Studies of genomic patterns, and their evolutionary underpinnings, continue to be augmented by the recent push to obtain additional full-genome sequences of related Caenorhabditis taxa. In the near future, we expect to see major advances with the onset of whole-genome resequencing of multiple wild individuals of the same species. In this review, we synthesize many of the important insights to date in our understanding of genome organization and function that derive from the evolutionary principles made explicit by theoretical population genetics and molecular evolution and highlight fertile areas for future research on unanswered questions in C. elegans genome evolution. We call attention to the need for C. elegans researchers to generate and critically assess nonadaptive hypotheses for genomic and developmental patterns, in addition to adaptive scenarios. We also emphasize the potential importance of evolution in the gonochoristic (female and male) ancestors of the androdioecious (hermaphrodite and male) C. elegans as the source for many of its genomic and developmental patterns.