Honeybees of the species Apis mellifera are important pollinators of crops and wild plants. Paenibacillus larvae , a spore-forming bacterium, is a problematic pathogen that causes American foulbrood (AFB) in honeybee larvae worldwide. In many countries, AFB is a notifiable disease, requiring the destruction of diseased colonies, resulting in economic loss that impacts beekeeping and agriculture. Disease onset starts with larval ingestion of P. larvae spores, which germinate into growing cells that proliferate in the larval gut, leading to larval death and eventually bee colony collapse. As infection progresses, P. larvae produce spores, reinitiating the disease cycle. Thus, growth, sporulation and germination underlie AFB. In this study, using various microbiological assays, quantitative cell biology methods, transmission electron microscopy and genomics, we sought to identify genetic and phenotypic characteristics associated with the predominant ERIC I and ERIC II genotypes of P. larvae during growth, sporulation and germination. Extending previous findings, our data identify genetic differences between ERIC I and ERIC II strains and some genetic variation between strains of the same ERIC type. Furthermore, we describe significant differences in cellular morphology during growth, differences in spore envelope structure and differences in germination efficiency between ERIC I and ERIC II genotypes. Collectively, our findings improve understanding of P. larvae biology and provide a foundation for developing genotype-specific disease management strategies for AFB.