I emailed Jonathon Goldman, the Dir. of Public Works and got a response. He wrote:
Good afternoon. Here's a short answer from MarinMap (attached). The pieces of roadway that have no zoning, are inside the City Limits (the red dashed line) and have no parcel boundaries crossing them are generally public right of way. Roads that transit parcels with a solid color (and are therefore not as visible on the attached), or have parcel boundaries across them or near the centerline are private and not publically-maintained. Wolfback Ridge Road, for example, has a public right of way part between US 101 and APN 064-276-22 (owned by the Marin Municipal Water District), a part that lies outside the City Limits and parts on private properties. Happy to try to answer any more specific questions. At some point, a land surveyor would be necessary to sort that all out.
The graphic he references is here: https://www.dropbox.com/s/hcsaclyxglbn1ih/Wolfback%20Zoning....
Honestly, I still can't tell which parts really are public and which parts aren't.