The team currently competes in the J2 League, Japanese second tier of professional football, hosting their home matches in the JIT Recycle Ink Stadium, located in Kōfu.

The name alludes to the famous phrase Fū-rin-ka-zan (風林火山) that Takeda Shingen, a prominent Kōfu-based daimyō in the Sengoku period, emblazoned on his war banners.

The club survived a difficult period between 1999 and 2001, when it suffered from financial troubles as well as miserable results on the pitch, including a streak of twenty-five consecutive losses.

They would beat Hokkaido Consadole Sapporo and Sagan Tosu away from home by 2–1 and 3–1 respectively to advance to the quarter finals, in a stage which they had been on 4 times without ever getting past it.

On 20 September 2023, Ventforet played their first AFC Champions League official match against Australian side Melbourne City for the competition's group stage.

Playing away at Melbourne Rectangular Stadium with few of their usual starting players, the match ended in a 0–0 draw, earning them their first point and clean sheet in this competition.

This marks the first time a team qualified for the knockout phase of the AFC Champions League though not playing in their nation's top division.