Evolutionary dynamics of the conflict between transposable elements (TEs) and their host genome remain elusive. This conflict would be intense in stress-adapted plants as stress can often reactivate TEs. Mangroves reduce TE load convergently in their adaptation to intertidal environments and thus provide a unique opportunity to address the host-TE conflict and its interaction with stress adaptation. Using the mangrove Rhizophora apiculata as a model, we investigated methylation and short interfering RNA (siRNA) targeting patterns in relation to the abundance and age of long terminal repeat (LTR) retrotransposons. We also examined LTR retrotransposons’ distance to genes, impact on neighboring gene expression, and population frequencies. We found differential accumulation among classes of LTR retrotransposons despite high overall methylation levels. This can be attributed to 24-nt siRNA-mediated CHH methylation preferentially targeting Gypsy elements, particularly in their LTR regions. Old Gypsy elements possess unusually abundant siRNAs which show cross-mapping to young copies. Gypsy elements appear to be closer to genes and under stronger purifying selection than other classes. Our results suggest a continuous host-TE battle masked by the TE load reduction in R. apiculata. This conflict may enable mangroves like R. apiculata to maintain genetic diversity and thus evolutionary potential during stress adaptation.