Multicellular organisms display an enormous range of life history strategies and present an evolutionary conundrum; despite strong natural selection, life history traits are characterized by high levels of genetic variation. To understand the evolution of life histories and the maintenance of this variation, the specific phenotypic effects of segregating alleles and the genetic networks in which they act need to be elucidated. In particular, the extent to which life history evolution is constrained by the pleiotropy of alleles contributing to life history variation is generally unknown. Here we review recent empirical results that shed light on this question, with an emphasis on studies employing genomic analyses. While genome-scale analyses are increasingly practical and affordable, they face limitations of genetic resolution and statistical power. We describe new research approaches that we believe can produce new insights and evaluate their promise and applicability to different kinds of organisms. Two approaches seem particularly promising: experiments that manipulate selection in multiple dimensions and measure phenotypic and genomic response, and analytical approaches that take into account genome-wide associations between markers and phenotypes, rather than applying a traditional marker-by-marker approach.