Ticks are primarily studied as vectors of human and veterinary pathogens, a perspective that has strongly oriented microbiome research toward a pathocentric and medical framework. While this approach has led to major advances in our understanding of tick-borne diseases, it also obscures the true diversity, structure, and ecological importance of tick-associated microbial communities. Beyond pathogens, ticks host a wide range of endosymbionts, often transmitted transovarially, which are an integral part of their biology and evolution. As strictly hematophagous and trophically ultra-specialized arthropods, ticks face severe nutritional constraints. Blood is notably deficient in essential B vitamins that ticks, like other arthropods, cannot de novo synthesize, creating a fundamental ecological dependence on bacterial partners. Obligate nutritional endosymbionts, primarily provisioning B vitamins and in some cases heme and chorismate, constitute a core component of the tick microbiome. By promoting the evolutionary adaptation of ticks to strict hematophagy, these endosymbionts favoured the radiation that gave rise to the >900 existing tick species. However, they often belong to genera that also include highly virulent intracellular vertebrate pathogens, which fuels recurrent confusion in molecular surveys and underscores the need for rigorous taxonomic and functional discrimination. Recognizing their mutualistic, non-infectious, role profoundly reshapes estimates of infection risk, which are likely lower than suggested by pathogen-centered approaches. In parallel, current research is increasingly focusing on facultative endosymbionts, non-essential bacteria whose prevalence may vary substantially among tick populations. Most exhibit strict intracellular lifestyles and highly specific tissue tropisms that differ from those of horizontally transmitted pathogens, reflecting predominant transovarial transmission. Some facultative endosymbionts may influence tick reproduction: recent genomic surveys have identified genes involved in reproductive parasitism, such as the cif gene pair associated with cytoplasmic incompatibility in Wolbachia, which also occur in multiple other bacterial endosymbiont genera, including Rickettsia and Rickettsiella commonly found in ticks. Other facultative symbionts may act as defensive partners, providing protection against natural enemies and modulating susceptibility to tick-borne pathogens. In this context, they can influence the ecological dynamics of tick populations and potentially reduce pathogen transmission to vertebrate hosts. This emerging field opens exciting avenues for understanding the ecological and evolutionary dynamics of tick microbiomes, with potential applications in vector control and disease mitigation.