Substantial efforts to characterize the structural and functional diversity of soil, plant and insect-associated microbial communities have illuminated the complex interacting domains of crop-associated microbiomes that contribute to agroecosystem health. As a result, plant-associated microorganisms have emerged as an untapped resource for combating challenges to agricultural sustainability. However, despite growing interest in maximizing microbial functions for crop production, resource efficiency and stress resistance, research has struggled to harness the beneficial properties of agricultural microbiomes to improve crop performance. Here, we introduce the historical arc of agricultural microbiome research, highlighting current progress and emerging strategies for intentional microbiome manipulation to enhance crop performance and sustainability. We synthesize current practices and limitations to managing agricultural microbiomes and identify key knowledge gaps in our understanding of microbe-assisted crop production. Finally, we propose research priorities that embrace a holistic view of crop microbiomes for achieving precision microbiome management that is tailored, predictive and integrative in diverse agricultural systems.