Bacteria use multigenerational memory based on coupled oscillations of cAMP levels and type IV pili (TFP) activity to adaptively adhere to surfaces. These oscillations create cells with a “surface-sentient” state intermediate between planktonic and sessile, characterized by coordinated surface motility suppression. This intermediate state drastically increases the number of surface nonmotile cells and correlates with a transition in family tree architectures toward exponential surface population growth. Our data support the idea that reversible attachment is vital for irreversible attachment. That is, repeated sensing, division, and detachment cycles create a planktonic population with robust cAMP–TFP-based memory of the surface, allowing cells to return to the surface progressively better adapted for sensing and attachment, ultimately dominating the surface ecology via exponential surface population increase.