In this paper I critically explore the possibility that the hope for engaging in democratic discourse and coalition-building across deep— potentially irreconcilable— moral, religious divisions in current U.S. public life depends less upon further calls for “more tolerance,” and instead in thinking creatively and transformatively about how to democratize and constructively utilize conflict and intolerance. Is it possible to distinguish between constructive and destructive forms of intolerance? If so, what are the prospects for re-orienting analysis of democratic practices and processes so that what typically appear as forms of simple intolerance (and thus, as candidates for marginalization or exclusion from political processes) might be reconceived and re-directed for the purposes of constructively transforming those practices and processes? Further, what would an analytical framework that aimed to distinguish and cultivate “healthy conflict” in contrast to degenerative or destructive conflict look like? How would such an approach facilitate efforts on the ground to recognize, understand and transform religiously-motivated conflict? I pose answers to these questions by bringing strands from the “religion in public life” debates that have unfolded over recent decades among ethicists and political philosophers into conversation with conflict transformation literature in peace studies. Bridging these resources will help to re-conceptualize basic assumptions about tolerance and conflict as a pivotal first step in constructively transforming conflicts motivated by, or identified with, moral commitments and religious identities.