Plants recognize biotic challengers and respond with the appropriate defense by utilizing phytohormone signaling and crosstalk. Despite this, microbes and insects have evolved mechanisms that compromise the plant surveillance system and specific defenses, thus ensuring successful colonization. In nature, plants do not experience insect herbivores and microbes in isolation, but in combination. Over time, relationships have developed between insects and microbes, varying on a continuum from no-relationship to obligate relationships that are required for both organisms to survive. While many reviews have examined plant-insect and plant-microbe interactions and the mechanisms of plant defense, few have considered the interface where microbes and insects may overlap, and synergies may develop. In this review, we critically evaluate the requirements for insect-associated microbes to develop synergistic relationships with their hosts, and we mechanistically discuss how some of these insect-associated microbes can target or modify host plant defenses. Finally, by using bioinformatics and the recent literature, we review evidence for synergies in insect-microbe relationships at the interface of plant-insect defenses. Insect-associated microbes can influence host-plant detection and/or signaling through phytohormone synthesis, conserved microbial patterns, and effectors, however, microbes associated with insects must be maintained in the environment and located in opportunistic positions.