Colonies of neotropical army ants of the genus Eciton Latreille offer some of the most captivating examples of intricate interactions between species, with hundreds of associated species already described in colonies of Eciton burchellii Westwood. Among this plethora of species found with Eciton colonies, two genera of staphylinid beetles, Ecitomorpha Wasmann, and Ecitophya Wasmann, have evolved to mimic the appearance and parallel the colouration of the most abundant ant worker cast. Here, we study for the first time the association of these ant-mimicking beetles with their ant host in an evolutionary and population genetics framework. The central emphasis is on colonies of E. burchellii, the only Eciton species that harbours both genera of ant-mimicking beetles. Phylogenetic and population structure analyses using the same mtDNA COI region (802 bp) for ants and beetles indicated that speciation patterns of the myrmecophiles were congruent with specialization to a particular Eciton (sub)species. Therefore, current taxonomic treatments of Eciton and its Ecitomorpha and Ecitophya associates need revision. Molecular clock analyses suggested that diversification of the Eciton hosts pre-date that of their guests, with a possible earlier association of Ecitophya (found with a large number of Eciton species) than with Ecitomorpha (found only with E. burchellii colonies). Population-level analyses revealed that patterns of diversification for the myrmecophiles are also consistent with specialisation to a particular host across broad geographical areas but not at small geographical scales, with gene flow within each species found between host colonies, even across landscape features that are strong barriers for Eciton female-mediated gene flow.