This full model change was designed to meet the needs of sporty model enthusiasts. The GSX-R (400) pairs the lightweight yet highly rigid Dual Cell-ALBOX Frame with a freshly engineered 4-stroke DOHC 400 cm³ engine equipped with the new Suzuki Advanced Three-way Cooling System (SATCS). This system helps to reduce the size of the engine while increasing cooling efficiency by liquid-cooling the cylinder head, air-cooling the cylinder block via fins, and oil-cooling the inside of the pistons. This model combines the Deca Piston Brake System (DPBS) of the previous generation with new floating torque links at the rear to realize a brake system with superb performance. The low center of gravity, mass centered between the wheels, and newly designed fairings that lower the frontal projection area help to both reduce air resistance at high speeds (CdA: 0.28) and enhance handling. Riders can choose between fully and half-faired styling depending on preference.

This full model change features a range of substantial advancements from the previous model. The riding performance of the GSX-R400 was further enhanced by adopting a liquid-cooled 4-stroke DOHC 400 cm³ engine incorporating a wide range of upgrades throughout, the Suzuki Power-up Exhaust System (SPES) that increases low- to mid-range torque, and the newly designed Dual Cell-ALBOX Frame that is approximately 50% more rigid than the previous frame. In addition, the sport production version that debuted at the same time also features a close-ratio transmission, single seat fairing, inner rod type front forks with both rebound and compression adjusters, and separate-tank rear shock absorbers capable of adjusting both rebound and compression damping force.

The GSX-R400R is noted for its aerodynamically sharp styling features, such as a compact dual-headlight with a built-in windscreen and strongly raked fairings. The R400R has the same aluminum double-cradle frame design of the GSX-R750, the top model of the series. The rigidity of this frame was increased and inverted front forks adopted for even greater stability. The valve train in the engine incorporates innovations such as independent rocker arms, and the intake system combines a straight intake with a downdraft slingshot carburetor for higher intake efficiency and response. The exhaust system also features a highly efficient manifold-type muffler. A production sport-spec model debuted at the same time.