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One way to visualize the evolutionary process by which species can change and adapt is by thinking of organisms as explorers of the space of all possible genetic combinations. Mutations are the fuel that propagate populations within this space, and natural selection can be thought of as the guiding principle that dictates the viability of each step. What determines whether an organism is selected or not is its phenotype. Therefore, in order to figure out the actual evolutionary potential of organisms it is essential to understand how phenotypes are constructed and how those constructions can evolve. During the history of life on Earth some lineages have evolved key novelties that drastically impacted how phenotypes can develop, and, therefore, how those lineages evolve. One of the most drastic novelties in organismal organisation was the evolution of multicellularity in the stem-lineage to animals. This novelty was followed by an impressive exploration of shapes and habits that make up some of the most exquisite and intriguing diversity populating our planet. In this thesis, I will particularly focus on two features of animal organisation that represented novelties that accompanied the evolution of multicellularity. First, I will explore the influence of the evolution of novel distal regulatory elements called enhancers on the evolution of gene regulatory networks. Regulatory networks control the spatiotemporal gene expression patterns that give rise to and define the individual cell types of multicellular organisms. In eumetazoa, enhancers play a key role in determining the structure of such networks, particularly the wiring diagram of “who regulates whom”. Mutations that affect enhancer activity can therefore rewire regulatory networks, potentially causing adaptive changes in gene expression. Here, I will present results from analyzing whole-tissue and single-cell transcriptomic and chromatin accessibility data from mouse to show that enhancers play an additional role in the evolution of regulatory networks: They facilitate network growth by creating transcriptionally active regions of open chromatin that are conducive to de novo gene evolution. I also show that open reading frames gradually acquire interactions with enhancers over macroevolutionary timescales, helping integrate genes—those that have arisen de novo or by other means—into existing regulatory networks. Taken together, these results highlight a dual role of enhancers in expanding and rewiring gene regulatory networks. Secondly, I will present how the separation of reproductive and somatic cells during the development of animals can influence evolutionary trajectories. The evolution of a germline-soma separation in animals has the implication that much of the genetic variation that arises in the body of an individual cannot be inherited. Because of that, the adaptive potential of non-heritable somatic mutations has received limited attention in traditional evolutionary theory. I will here show how the ability of a germline genotype to express a novel phenotype via non-heritable somatic mutations can be selectively advantageous, and that this advantage can channel evolving populations toward germline genotypes that constitutively express the phenotype. I will present the results of simulations of evolving populations of developing organisms with an impermeable germline-soma separation navigating a minimal fitness landscape. Those simulations revealed the conditions under which non-heritable somatic mutations promote adaptation. Specifically, this can occur when the somatic mutation supply is high, when few cells with the advantageous somatic mutation are required to increase organismal fitness, and when the somatic mutation also confers a selective advantage at the cellular level. These results therefore provide proof-of-principle that non-heritable somatic mutations can promote adaptive evolution. These discoveries have important implications for how we understand the evolutionary potential of organisms, showing how the evolution of complex molecular mechanisms can facilitate the evolution of completely novel biochemical components, and how the ontological configuration of an organism can guide the evolutionary trajectories of its lineage. I conclude by emphasizing the importance of developmental and historical processes for the understanding of biological evolution.