Partial configuration of programmable circuitry with validation for an integrated circuit is described. An integrated circuit with programmable circuitry is obtained. The programmable circuitry is configured with a first bitstream in a non-dynamic mode of operation, after which the integrated circuit includes a configuration controller coupled to a buffer, an internal configuration access port, and an error checker. A portion of a second bitstream is loaded into the buffer for a dynamic partial configuration mode of operation. The portion of the second bitstream loaded into the buffer is validated with the error checker as being acceptable, after which the portion of the second bitstream is instantiated in the programmable circuitry via the internal configuration access port.