All sensory modalities serve a similar objective, which is to decode input by making predictions in time and space about an animal’s surroundings. The evolution of sensory modalities is driven by the need to shape effective behavioural outputs, and in turn increase survival. Throughout evolution, sensory systems have undergone a great deal of specialization; and even though some modalities are derived from unique origins within different phyla, they still exhibit many common design features (Strausfeld and Hildebrand 1999; Eisthen 2002; Jacobs et al. 2007). We now have detailed mechanistic data on how sensory systems operate within specific animals (Buck and Axel 1991; Chalasani et al. 2007; Sato et al. 2008; Wicher et al. 2008), however it is still not clear how sensory signalling pathways evolve at the molecular level, and whether these evolutionary mechanisms are shared between diverse taxa. Here we set out to investigate the molecular evolution of signalling pathway members across olfactory, gustatory, and photosensory modalities from very divergent phyla in an attempt to develop a model of molecular evolution for sensory systems. From our pairwise intraphylum analysis we found that sensory signalling pathways unusually undergo high levels of functional constraint that are higher than genomewide global levels of constraint, and this purifying selection is common within the very divergent taxa we examined. We also find that gene duplication events represent a conserved but heterogeneous driver of evolution within sensory signalling pathways. Taken together, we propose a ‘sessile’ mechanism of sensory signalling pathway evolution, which on one side facilitates bursts of gene duplication and relaxed selection and on the other side it is unusually anchored by high levels of selective constraint that preserves core sensory function.