Ecological divergence is a main source of trait differences between closely related species. Despite its importance in generating biodiversity, the genetic architecture of most ecologically relevant traits is poorly understood. In plants, differences in elevation can impose substantial selection for phenotypic divergence of both complex, correlated suites of traits (such as life history), as well as novel adaptations. Here, we use the Mimulus guttatus species complex to assess if divergence in elevation is associated with trait divergence in a group of closely related perennial species, and determine the genetic architecture of this divergence. We find that divergence in elevation is associated with both differences in multivariate quantitative life history traits, as well as a unique trait; the production of belowground stolons, but the extent of phenotypic divergence among species depends on ontogeny. We show that the genetic architecture of this divergence between two perennial species is simple, involving few mid to large effect Quantitative Trait Loci (QTLs). Lastly, we discover that the genetic architecture of the ability to produce belowground stolons changes through development. In sum, perennials of the M. guttatus species complex exhibit substantial phenotypic divergence, which is associated with elevational differences, and is controlled by few genetic changes.