[3][4] It had an air-cooled, transverse-mounted 408 cc (24.9 cu in) inline four-cylinder engine with two valves per cylinder operated by a single chain-driven overhead camshaft.

[6]: 112  In order to develop the CB350F into the CB400F, Honda increased the bore and modified the cylinder head to raise the compression ratio.

[8] But what the CB400F engine lacked in power it made up for in refinement, the small-displacement four-stroke being smoother, quieter and much more economical than the two-strokes.

They praised its renewed focus over the previous 350F model, preferring its clean lines and sporty café racer looks.

[2]: 42 To comply with licence restrictions in France and Japan, Honda also produced a 398 cc (24.3 cu in) version by fitting a shorter 48.8 mm (1.92 in) stroke crankshaft.

Kaz Yoshima, a former employee at Honda's R&D department in Japan,[12]: 65  built 492 cc (30.0 cu in) race versions capable of 13,500 rpm and producing an estimated 60 bhp (45 kW).

[12]: 66  Ron Haslam won the 1980 Formula 3 title on a CB400F prepared by Honda dealer Nettleton Motorcycles.

[13] In late 2011 a UK-based company, David Silver Spares, announced they would be acquiring used CB400Fs to restore and resell to the public.