High-throughput sequencing technologies have greatly advanced our understanding of microbiomes, but resolving microbial communities at species and strain levels remains challenging. In this study, we present a pipeline for designing, multiplexing, and sequencing highly polymorphic taxon-specific amplicons using PacBio circular consensus sequencing. We focus on the wheat microbiome as a proof-of-principle and demonstrate unprecedented resolution for the wheat-associatedPseudomonasmicrobiome and the ubiquitous fungal pathogenZymoseptoria tritici. Our approach achieves an order of magnitude higher phylogenetic resolution compared to existing ribosomal amplicons. We show that the designed amplicons accurately capture species and strain diversity outperforming full-length 16S and ITS amplicons. We track microbial communities in the wheat phyllosphere across time and space to establish fine-grained species and strain-specific dynamics. The high-resolution profiling provided by taxon-specific amplicons opens new avenues for studying microbial community dynamics in complex environments. Moreover, the cost-effectiveness and scalability of our approach make it applicable to diverse ecological studies. Overall, our work demonstrates the potential of long-read amplicon sequencing to overcome limitations in phylogenetic resolution and enhance our understanding of microbiome diversity and dynamics.