diff --git a/sshuttle/client.py b/sshuttle/client.py
index da23b7d..ab28d0b 100644
--- a/sshuttle/client.py
+++ b/sshuttle/client.py
@@ -589,7 +589,7 @@ def main(listenip_v6, listenip_v4,
     # redirect packets outgoing to this server to the remote host
     # instead.
     if dns:
-        nslist += resolvconf_nameservers()
+        nslist += resolvconf_nameservers(True)
         if to_nameserver is not None:
             to_nameserver = "%s@%s" % tuple(to_nameserver[1:])
     else:
diff --git a/sshuttle/helpers.py b/sshuttle/helpers.py
index 5d61b43..0cd97df 100644
--- a/sshuttle/helpers.py
+++ b/sshuttle/helpers.py
@@ -48,10 +48,18 @@ class Fatal(Exception):
     pass
 
 
-def resolvconf_nameservers():
-    """Retrieves a list of tuples (address type, address as a string) that
-    the current system uses to resolve hostnames from /etc/resolv.conf
-    and possibly other files.
+def resolvconf_nameservers(systemd_resolved):
+    """Retrieves a list of tuples (address type, address as a string) of
+    the DNS servers used by the system to resolve hostnames.
+
+    If parameter is False, DNS servers are retrieved from only
+    /etc/resolv.conf. This behavior makes sense for the sshuttle
+    server.
+
+    If parameter is True, we retrieve information from both
+    /etc/resolv.conf and /run/systemd/resolve/resolv.conf (if it
+    exists). This behavior makes sense for the sshuttle client.
+
     """
 
     # Historically, we just needed to read /etc/resolv.conf.
@@ -59,10 +67,10 @@ def resolvconf_nameservers():
     # If systemd-resolved is active, /etc/resolv.conf will point to
     # localhost and the actual DNS servers that systemd-resolved uses
     # are stored in /run/systemd/resolve/resolv.conf. For programs
-    # that use the localhost DNS server, only reading /etc/resolv.conf
-    # is sufficient. However, resolved provides other ways of
-    # resolving hostnames (such as via dbus) that may not route
-    # requests through localhost. So, we retrieve a list of DNS
+    # that use the localhost DNS server, having sshuttle read
+    # /etc/resolv.conf is sufficient. However, resolved provides other
+    # ways of resolving hostnames (such as via dbus) that may not
+    # route requests through localhost. So, we retrieve a list of DNS
     # servers that resolved uses so we can intercept those as well.
     #
     # For more information about systemd-resolved, see:
@@ -70,7 +78,9 @@ def resolvconf_nameservers():
     #
     # On machines without systemd-resolved, we expect opening the
     # second file will fail.
-    files = ['/etc/resolv.conf', '/run/systemd/resolve/resolv.conf']
+    files = ['/etc/resolv.conf']
+    if systemd_resolved:
+        files += ['/run/systemd/resolve/resolv.conf']
 
     nsservers = []
     for f in files:
@@ -90,8 +100,12 @@ def resolvconf_nameservers():
     return nsservers
 
 
-def resolvconf_random_nameserver():
-    lines = resolvconf_nameservers()
+def resolvconf_random_nameserver(systemd_resolved):
+    """Return a random nameserver selected from servers produced by
+    resolvconf_nameservers(). See documentation for
+    resolvconf_nameservers() for a description of the parameter.
+    """
+    lines = resolvconf_nameservers(systemd_resolved)
     if lines:
         if len(lines) > 1:
             # don't import this unless we really need it
diff --git a/sshuttle/server.py b/sshuttle/server.py
index 8e15866..67409a7 100644
--- a/sshuttle/server.py
+++ b/sshuttle/server.py
@@ -205,7 +205,7 @@ class DnsProxy(Handler):
         self.tries += 1
 
         if self.to_nameserver is None:
-            _, peer = resolvconf_random_nameserver()
+            _, peer = resolvconf_random_nameserver(False)
             port = 53
         else:
             peer = self.to_ns_peer
diff --git a/tests/client/test_helpers.py b/tests/client/test_helpers.py
index 3ed588f..732f38a 100644
--- a/tests/client/test_helpers.py
+++ b/tests/client/test_helpers.py
@@ -131,7 +131,7 @@ nameserver 2404:6800:4004:80c::3
 nameserver 2404:6800:4004:80c::4
 """)
 
-    ns = sshuttle.helpers.resolvconf_nameservers()
+    ns = sshuttle.helpers.resolvconf_nameservers(False)
     assert ns == [
         (AF_INET, u'192.168.1.1'), (AF_INET, u'192.168.2.1'),
         (AF_INET, u'192.168.3.1'), (AF_INET, u'192.168.4.1'),
@@ -156,7 +156,7 @@ nameserver 2404:6800:4004:80c::2
 nameserver 2404:6800:4004:80c::3
 nameserver 2404:6800:4004:80c::4
 """)
-    ns = sshuttle.helpers.resolvconf_random_nameserver()
+    ns = sshuttle.helpers.resolvconf_random_nameserver(False)
     assert ns in [
         (AF_INET, u'192.168.1.1'), (AF_INET, u'192.168.2.1'),
         (AF_INET, u'192.168.3.1'), (AF_INET, u'192.168.4.1'),