Plant viruses are widespread in nature, where they operate in intimate association with their hosts and often with vectors. Most research on plant viruses to the present has focused on agricultural systems (agronomic and horticultural) and viruses that are pathogenic. Consequently, there is a dearth of fundamental information about plant virus dynamics in natural ecosystems and how they might differ from or be influenced by virus interactions in managed systems. Key questions include under what conditions the influence of virus on host fitness is negative, neutral, or positive and the extent to which this relationship is influenced by ecosystem properties. To address these critical knowledge gaps, the expanding field of plant virus ecology seeks to examine (i) the ecological roles of plant-associated viruses and their vectors in managed and unmanaged ecosystems and (ii) the reciprocal influence of ecosystem properties on the distribution and evolution of plant viruses and their vectors. In this work, plant virus ecology draws on the achievements of epidemiology and extends the research focus to new ecological arenas. Here we provide an historical perspective and highlight key issues and emerging research directions. We suggest that there is broad need to (i) integrate consideration of plant viruses into ecological research and theory, in which viruses have generally been overlooked, and (ii) to expand ecological perspectives in virology to include new methods and disciplines in ecology, such as ecosystem ecology. Studies of plant-virus-vector interactions in nature offer both opportunities and challenges that will ultimately produce multi-faceted understanding of the role of viruses in shaping ecological and evolutionary dynamics. Copyright © 2011 Elsevier B.V. All rights reserved.