AbstractAim To understand the evolution of long‐distance temperate–tropical migration in a South American bird, Swainson's flycatcher (Myiarchus swainsoni).Methods A total of 842 base pairs of the mitochondrial DNA genes ATPase 8 and 6 were sequenced from forty‐nine individuals of the M. swainsoni complex from most of its range. Analyses measured the phylogenetic signal in the data, and tools of population genetics, phylogeography and phylogeny were used to interpret the evolution of the bird and its migration on the South American landscape.Results Migratory populations in the M. swainsoni complex are not each other's closest relatives. The migratory subspecies M. s. swainsoni, which breeds in south‐eastern South America, is not closely related to the rest of the complex. The remaining migratory populations of the subspecies M. s. ferocior and two intergrade populations are extremely closely related to non‐migratory populations with which they form a well‐supported clade despite substantial morphological differentiation from each other. Within this clade of migrants and non‐migrants, net divergence across 4000 km of lowland South America is zero and most diversity is distributed among individuals not populations. Mismatch analyses and significant values of Tajima's D and Fu's Fs suggest the clade has undergone a very recent range expansion. Migration and the shifts of breeding distribution that accompanied its evolution evolved twice within what has recently been considered the polytypic species M. swainsoni. Furthermore, these shifts of range probably occurred at very different times as parts of different southward ‘pulses’ of humid, Amazonian taxa.Main conclusions Evolution of temperate‐tropical migration in the M. swainsoni complex has been spatio‐temporally layered on the South American landscape. The analysis cautions that the historical biogeography underlying a single present‐day migration system need not have been driven by a single set of environmental factors operating at one time. We suggest directions for further study of ecology and demography in zones of apparent contact between various migratory and non‐migratory populations.