The Steam Controller sold out within about 30 minutes after going on sale on May 4 at the price of $99. The Steam store page initially listed a delivery window of three to five business days, which later extended to six to ten days before the product was marked as out of stock. Valve has not provided an update on when new units will be available, although some users reported brief reappearances of the controller before it sold out again.

Scalpers acted quickly, with eBay listings ranging from $200 to $280 for most units. The highest listed price currently stands at $556, representing a 461% markup over Valve's retail price.

Some sellers are also listing older original Steam Controllers alongside Steam Link bundles, likely to take advantage of search traffic generated by the launch.

Reviews published around launch have been largely positive, praising the controller's comfort, dual trackpads, gyro controls, TMR magnetic thumbsticks, four rear grip buttons, and the Grip Sense feature, which detects where the player's hands are touching the controller.

The $99 price and reliance on Steam's ecosystem are the main criticisms. Valve's programmer Pierre-Loup Griffais and mechanical engineer Steve Cardinali told Tom's Hardware that the controller was developed based on how Steam Deck users were using the device docked to a TV, often losing access to the built-in inputs. The Steam Controller aims to replicate that layout in a standalone design.

On Windows and macOS, the controller mainly acts as a mouse and keyboard input device unless Steam is running. Valve chose not to develop a kernel-level driver for these systems, citing concerns over system stability. Linux, on the other hand, has native kernel support for gamepads. As a result, the Steam Controller is less versatile as a universal gamepad outside of Steam compared to Xbox or PlayStation controllers.

The included Puck accessory functions as both a wireless receiver and a charging dock. Valve states that the custom wireless protocol can support up to four controllers at the same time without the latency issues sometimes associated with multiple Bluetooth connections.