Coevolution is predicted to depend on how the genetic diversity of
interacting species is geographically structured. Plant-microbe
symbioses such as the legume-rhizobium mutualism are ecologically and
economically important, but distinct life history and dispersal
mechanisms for these host and microbial partners, plus dynamic genome
composition in bacteria, present challenges for understanding spatial
genetic processes in these systems. Here we study the model rhizobium
Ensifer meliloti using a hierarchically-structured sample of 191 strains
from 21 sites in the native range and compare its population structure
to that of its host plant Medicago truncatula. We find high local
genomic variation and minimal isolation by distance across the rhizobium
genome, particularly at the two symbiosis elements pSymA and pSymB,
which have evolutionary histories and population structures that are
similar to each other but distinct from both the chromosome and the
host. While the chromosome displays weak isolation by distance, it is
uncorrelated with hosts. Patterns of discordant population structure
among elements with the bacterial genome has implications for bacterial
adaptation to life in the soil versus symbiosis, while discordant
population genetic structure of hosts and microbes might restrict local
adaptation of species to each other and give rise to phenotypic
mismatches in coevolutionary traits.