The growing non-religious minority remains among the most distrusted groups in America. We examined how non-religious individuals experience microaggressions—subtle prejudicial verbal and behavioral acts. U.S. participants who self-identified as being non-religious (N = 1,485) were recruited to develop and validate a Microaggressions Against Non-religious Individuals Scale (MANRIS). Items from MANRIS were created using prior literature, expert feedback, and psychometric assessment. An exploratory factor analysis (n = 765) yielded a 31-item, five-factor model: Assumption of Inferiority, Denial of Non-religious Prejudice, Assumption of Religiosity, Endorsing Non-religious Stereotypes, and Pathology of a Non-religious Identity. A confirmatory factor analysis (n = 720) supported a bifactor five-factor model. Both studies produced high levels of internal consistency, cumulative variance, and fit. We found experiences of non-religious microaggressions to uniquely predict depressive symptoms, even after controlling for potential confounds including overt non-religious discrimination. Atheists reported experiencing the highest incidences of non-religious microaggressions and discrimination compared to other non-religious groups. We discuss the applications of the scale in light of the broader discussions and criticism about microaggressions.