/etc/resolv.conf is the file which contains the list of DNS servers to query. The first IP listed is the primary name server, the second is the secondary nameserver, the third is the tertiary nameserver.
It is generally non-sensical to have different nameservers for different interfaces, but there are a few applications.
Generally this is accomplished by running a caching DNS server on the local network which has zone transfer capabilities for domains on the "other" network so that it can service both. Often this caching nameserver is run on the gateway computer that is attached to both networks.
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