Direct proof of use
The F-35 Lightning II is directly documented in the 2001 War in Afghanistan through the U.S. Marine Corps F-35B combat strike on September 27, 2018. U.S. Naval Forces Central Command reported that Marine Corps F-35Bs conducted the strike in the U.S. Central Command area of responsibility in support of Operation Freedom's Sentinel in Afghanistan.
The same official account says the mission was an air strike supporting ground-clearance operations and that the ground force commander deemed the strike successful. DVIDS separately identifies two VMFA-211 F-35B Lightning II aircraft from the 13th Marine Expeditionary Unit conducting aerial refueling with a U.S. Air Force KC-135 during a combat mission over Afghanistan on the same date.
Sources: NAVCENT F-35B First Combat Strike, DVIDS F-35s Fly First Combat Mission
Timeline
The documented Afghanistan use centers on a single public milestone: September 27, 2018. Before the strike, VMFA-211 F-35Bs were embarked on USS Essex as part of the Essex Amphibious Ready Group and 13th Marine Expeditionary Unit.
On that date, official imagery shows Marines loading ordnance into an F-35B aboard USS Essex in preparation for the F-35B's first combat strike. The strike was then flown in support of Operation Freedom's Sentinel in Afghanistan, with DVIDS video metadata placing VMFA-211 F-35Bs over Afghanistan during the combat mission.
Sources: CENTCOM F-35B Strike Preparation Image, NAVCENT F-35B First Combat Strike, DVIDS F-35s Fly First Combat Mission
Operational role
In the Afghanistan record, the F-35B appears as a U.S. Marine Corps strike aircraft supporting U.S.-led and Afghan government operations rather than as a system transferred to Afghan forces. The public sources identify VMFA-211, the 13th Marine Expeditionary Unit, USS Essex, and Operation Freedom's Sentinel; they do not provide a public target name, strike location inside Afghanistan, munition type, or battle-damage details.
The evidence supports cataloging the aircraft on the United States, NATO, and Afghan government side of the war with long-range strike and fire-support roles. The sources describe the mission as air support to ground-clearance operations from the Essex Amphibious Ready Group, not routine basing inside Afghanistan.
Sources: NAVCENT F-35B First Combat Strike, DVIDS F-35s Fly First Combat Mission, CENTCOM F-35B Strike Preparation Image