A system may include an electronic device such as a head-mounted device and a handheld controller for controlling the electronic device. The handheld controller may have a housing with an elongated shaft extending between first and second tip portions. The handheld controller may have power receiving circuitry configured to receive power from a power source. The power source may be incorporated into an electronic device such as a wireless charging dock or stick, a battery case, or a head-mounted device. The power source may supply power through terminals that form ohmic contacts with mating terminals in the finger device or may transmit power wirelessly using capacitive coupling or inductive charging arrangements. Magnets may be used to hold and align the elongated shaft of the handheld controller on the power source.