Meeting the challenges of visually sampling an ancient aquatic landscape by the early vertebrates was crucial to their survival and would establish a photoreceptive bauplan to be used by all subsequent vertebrate descendents. Image-forming eyes were under tremendous selection pressure and the ability to identify suitable prey and detect potential predators was thought to be one of the major drivers of speciation in the Early Cambrian. Using extant representatives of the earliest stage in vertebrate evolution (lampreys), we have investigated the evolution and development of photoreception (image formation and irradiance detection) at both the peripheral (visual and non-visual tissues of the body) and the central (optic tectum and pineal organ) nervous systems. Using anatomical, electrophysiological and molecular approaches to measure photoreceptive capacity, we explored the environmental drivers of visual behavior in these ancient vertebrates. Our results reveal that lampreys possess complex visual and non-visual photoreceptive systems, with well-developed eyes with the potential for at least tetrachromatic colour discrimination and photoreceptive cells in the pineal organ, that are able to provide chromatic input to set circadian levels of activity. We also reveal that the input to the optic tectum and pineal organ also varies over the adult lamprey lifecycle, where ecological factors such as light conditions and habitat exert a significant influence on brain structure size and consequently on behavioural activity patterns. This work offers a unique opportunity to understand how phylogenetic constraints and environmental signals influence the development of the visual pathway in an ancient vertebrate that has existed for over 500 million years.