The vertebrate filamin family (A, B, and C) are critically involved in development of brain structure, cardio-vasculature, and skeleton. Filamins are large F-actin cross-linking proteins containing an actin-binding domain, followed by 24 Immunoglobulin(Ig)-like domains. Filamins play critical cellular roles as mechanical and scaffold proteins. As mechanical proteins they cross-link F-actin into gels or fibrils. As scaffold proteins they bind over 70 critical proteins. Filamins have overlapping and distinct roles, however it is not understood why. Nor well understood, are the mechanisms by which filamin act as mechanical proteins. Our work focuses on understanding their function; by analyzing site-specific functional divergence, using the evolutionary trace (ET) method, over vertebrate developmental periods --- Teleostei, Amphibian, and Mammalian; and by analyzing filamin behavior under mechanical stress. We find, isoforms diverge from one gene between urochordate and vertebrate lineages; most divergence occurs in Teleostei; and that filamin C diverged least. In addition, the heterogeneous spatial pattern of functional divergence we observe is not correlated with scaffold protein activity either in binding interfaces or across domains. Our results also suggest isoforms have diverged with regard to specificity for binding partners or regulatory function. To elucidate the structure-function relationship of filamin, we used constant force (0-315 pN) simulations to derive both the critical unfolding force and the unfolding pathways at biological levels of force (35-70 pN). Despite a large heterogeneity in the population of force-induced intermediate states, we find a common initial unfolding intermediate in all the Ig-like domains of filamin, where the N-terminal [beta] strand unfolds. We also study the simulated thermal unfolding of several filamin Ig-like domains. We find that thermally-induced unfolding has an early-stage intermediate state similar to the one observed in force-induced unfolding and characterized by the N-terminal strand being unfurled. We propose that the N-terminal strand may act as a conformational switch that unfolds under physiological forces leading to exposure of cryptic binding sites, removal of native binding sites, and modulating the quaternary structure of domains. This work provides insights into both isoform distinctive and mechanical properties of vertebrate filamin.