Exposure to environmental particles during pregnancy increases asthma susceptibility of the offspring. We tested the hypothesis that this transmission continues to F2 and F3 generations and occurs via epigenetic mechanisms. We compared allergic susceptibility of three generations of BALB/c offspring after a single maternal exposure during pregnancy to diesel exhaust particles or concentrated urban air particles. After pregnant dams received intranasal instillations of particle suspensions or control, their F1, F2 and F3 offspring were tested in a low-dose ovalbumin protocol for allergy sensitivity. We found that the elevated asthmatic susceptibility after maternal exposure to particles during pregnancy persists into F2 and, with lesser magnitude, into F3 generations. This was evident from elevated eosinophil counts in bronchoalveolar lavage fluid (BAL), histopathologic changes of allergic airway disease, and increased BAL levels of IL-5 and IL-13. We have previously shown that dendritic cells (DCs) can mediate transmission of risk upon adoptive transfer. We therefore used an enhanced reduced representation bisulfite sequencing protocol to quantify DNA methylation in DCs from each generation. Distinct methylation changes were identified in F1, F2 and F3 DCs. The subset of altered loci shared across the 3 generations were not linked to known allergy genes or pathways, but included a number of genes linked to chromatin modification, suggesting potential interaction with other epigenetic mechanisms (e.g. histone modifications).The data indicate that pregnancy airway exposure to DEP triggers a transgenerationally transmitted asthma susceptibility and suggests a mechanistic role for epigenetic alterations in DCs in this process.