The mutualistic lifestyle of pollinating fig wasps and fig trees provides an excellent model for studying ecological and adaptive evolution issues. Transposable elements (TEs), as an important component of the genomes, are powerful driver for organisms to adapt to environment. Here, the genomic TEs of six pollinating fig wasps and five non-pollinating fig wasps were analyzed in the characteristics of composition and their effects on genome size, the historical burst patterns and their association with effective population size and paleoclimate changes, to infer the role of TEs in environmental adaptation in fig wasps. Compared with non-pollinators, pollinators’ TEs showed a significantly different burst state with less types and amount, shorter lengths, and lower contents in the genomes. The recent smaller effective population size and contractive demography failed to cause pollinators to accumulate more TEs, while the large number of TEs accumulated in non-pollinators positively correlated with their population expansion. The major TEs burst peaks in the history of pollinators highly overlapped with the warmer times in the Coolhouse in geological history. TEs located in the major peak period were mostly inserted near genes related to environment information processing such as Circadian entrainment pathway, and might act as CRMs (cis-regulatory modules) to regulate the conjunctive genes in response to paleoclimate changes in pollinators. These results revealed the molecular basis of the fig wasp’s response to changes in the syconia microenvironment and paleoclimate macroenvironment from the perspective of genomic TEs.