Erwinia amylovora is the causal agent of fire blight, which affects apple and pear. E. amylovora primarily suppresses host defenses using type III secretion effectors. It then forms biofilms within the xylem vessels, eventually leading to shoot blight. The ubiquitous bacterial second messenger cyclic-di-GMP (c-di-GMP) enables E. amylovora to transition between these infective stages by regulating several critical virulence factors including Type III secretion and biofilm formation. Intracellular levels of c-di-GMP are modulated by the targeted hydrolysis action of phosphodiesterases, PdeA, PdeB and PdeC. The combined deletion of pdeA, pdeB and pdeC in E. amylovora results in significantly elevated intracellular levels of c-di-GMP, resulting in an autoaggregating cell behavior, that impacts biofilm formation and cell separation post septation. We screened a library of transposon mutants generated in E. amylovora Ea1189?pdeABC for suppression of this autoaggregation phenotype. We identified a peptidoglycan hydrolase encoding gene eagA (Erwinia aggregation factor A), that is involved in the regulation of autoaggregation under high intracellular levels of c-di-GMP. eagA, is located downstream of, and co-regulated with znuA, the zinc-binding transporter component of the ZnuABC high-affinity zinc uptake system. Our results suggest that EagA responds to a localized intracellular pool of c-di-GMP generated at elevated Zn²⁺ concentrations by diguanylate cyclase DgcE, and positively regulates the expression of znuA. EagA also positively impacts E. amylovora virulence in apple shoots.