A Dynamic Host Configuration Protocol (DHCP) communications configuration system includes a client information handling system (IHS) coupled to a controller over a network. The client IHS creates a plurality of DHCP discover messages that include capability data that describes at least one hardware resource on the client IHS, and sends the plurality of DHCP discover messages over the network. The controller receives the plurality of DHCP discover messages and processes the capability data to determine configuration data for the client IHS, creates a plurality of DHCP offer messages including the configuration data for the client IHS, and sends the plurality of DHCP offer messages over the network to the client IHS. The client IHS then uses the configuration data to configure the client IHS.