The symbiotic relationship between corals and symbiodiniaceans can favor reef formation, but is easily rupted when these organisms are exposed to thermal anomalies. Here, we assessed the ITS2 rDNA phylotype diversity of dominant Symbiodiniaceae lineages associated with the hydrocoral Millepora alcicornis and investigated host–symbiont distribution patterns in the Atlantic Ocean. This is the first effort to assess the symbiont community of this hydrocoral over nearly its entire distributional range. Millepora alcicornis is highly generalist in the composition of its photosymbiont community. We found 16 ITS2 phylotypes, mainly of the genus Breviolum but also of the genera Symbiodinium and Cladocopium; nine of them are new lineages. The distribution patterns of the M. alcicornis–Symbiodiniaceae associations were explained by differences in primary productivity, photosynthetically active radiation, water turbidity, and temperature. Six geographic sections were identified. Colonies from the Brazilian Northeastern Region showed the most stable associations, with two Breviolum phylotypes, while those from the Brazilian Eastern Region showed the most diverse symbiont community, composed of three genera of Symbiodiniaceae. A new and dominant phylotype of Breviolum was identified in the Brazilian Southern Region. Our results suggest a radiation of Breviolum lineages associated with M. alcicornis through the Atlantic Ocean. The impressive diversity of symbiotic associations observed characterizes an adaptable host–symbiont relationship, which can be key for colonization of new habitats and the resilience of milleporids to environmental changes.