A three-degrees-of-freedom aeroelastic system with concentrated structural nonlinearities is considered. The aerodynamic loads in the model are simulated by using unsteady aerodynamic forces. First, we evaluate the linear stability region of the aerodynamic system employing the Lienard–Chipart criterion so that the stability boundaries of the center of gravity position and the uncoupled pitch natural frequency are obtained. Next, we present the distribution of the first Lyapunov coefficient l1 in the parameter space by using the Poincaré projection method to determine the type of Hopf bifurcation (subcritical or supercritical). We identify three types of hysteresis loops associated with Hopf bifurcations: the first type contains one stable equilibrium point and one stable limit cycle, the second type consists of one stable equilibrium point and two stable limit cycles, and the third type comprises two stable limit cycles. Nonlinear analysis shows that the variations in hysteresis loop types are mainly caused by the nonlinear flutter critical points, namely the saddle–node bifurcation points of limit cycles. Furthermore, we determine a degenerate Hopf bifurcation type known as generalized Hopf bifurcation (Bautin bifurcation) and its corresponding second Lyapunov coefficient, l2. Subsequently, we conduct nonlinear flutter analyses for positive and negative values of l2 by using bifurcation diagrams and phase portraits. The results show that when the uncoupled pitch natural frequency is used as the control parameter, the occurring generalized Hopf bifurcations are all supercritical (l2<0). However, when the center of gravity position is used as the control parameter, the generalized Hopf bifurcations that occur have both supercritical and subcritical (l2>0) modes.