Developing landscape design principles for the provision of ecosystem services is crucial to efficient and widespread implementation of environmental service-based projects. We investigate optimal farm design for agricultural pollination services from bees nesting in native habitat, integrating ecological and economic approaches in a spatial modeling framework. We evaluate the simplest case, and then add consideration of bee metapopulation dynamics and heterogeneity in farmland productivity. We find that the need for spatially even pollination coverage across farms means that bee habitat is often denser at the edges, rather than the centers, of optimally designed farms, and also highly constrains the ability of farmers to site bee habitat in less-productive areas of farms with spatial gradients in agricultural fertility. Optimal farm configuration is not purely a matter of uniform size and spacing of bee habitat: in some circumstances, farms combine large parcels—to ensure bee population persistence—with smaller, dispersed patches to provide spatially continuous pollination services. The highest-yield farm designs are those with a relatively small (but non-zero) area of pollination reservoirs, suggesting a conservation strategy of small parcels of service-providing habitat interspersed throughout working landscapes. The design principles outlined here are likely general and applicable to other ecosystem services supplied at local scales, such as agricultural pest control.