diff --git a/dns/asyncquery.py b/dns/asyncquery.py
index 7e9b886a..43c42caf 100644
--- a/dns/asyncquery.py
+++ b/dns/asyncquery.py
@@ -732,7 +732,7 @@ async def _http3(
     if url_parts.port is not None:
         port = url_parts.port
 
-    q.id = 0
+    q.set_id(0)
     wire = q.to_wire()
     the_connection: dns.quic.AsyncQuicConnection
     if connection:
@@ -804,7 +804,7 @@ async def quic(
     if server_hostname is not None and hostname is None:
         hostname = server_hostname
 
-    q.id = 0
+    q.set_id(0)
     wire = q.to_wire()
     the_connection: dns.quic.AsyncQuicConnection
     if connection:
diff --git a/dns/asyncresolver.py b/dns/asyncresolver.py
index c18ad0b1..2b8f6d97 100644
--- a/dns/asyncresolver.py
+++ b/dns/asyncresolver.py
@@ -89,6 +89,7 @@ async def resolve(
                 nameserver, tcp, backoff = resolution.next_nameserver()
                 if backoff:
                     await backend.sleep(backoff)
+                request.set_random_id()
                 timeout = self._compute_timeout(start, lifetime, resolution.errors)
                 try:
                     response = await nameserver.async_query(
diff --git a/dns/message.py b/dns/message.py
index 1cacb786..d514e56c 100644
--- a/dns/message.py
+++ b/dns/message.py
@@ -801,6 +801,25 @@ def had_tsig(self) -> bool:
     def _make_opt(flags=0, payload=DEFAULT_EDNS_PAYLOAD, options=None):
         return dns.renderer._make_opt(flags, payload, options)
 
+    def set_id(self, id: int):
+        """Set the message id to the specified value, and if TSIG is going to be used
+        to sign this message later, update it accordingly.
+
+        :param id: The message id
+        :type id: int
+        """
+        self.id = id
+        if self.want_tsig_sign:
+            assert self.tsig is not None
+            assert self.tsig.rdtype == dns.rdatatype.TSIG
+            tsig_rdata = cast(dns.rdtypes.ANY.TSIG.TSIG, self.tsig[0])
+            self.use_tsig(self.keyring, None, tsig_rdata.fudge, id, tsig_rdata.error, tsig_rdata.other,
+                          tsig_rdata.algorithm)
+
+    def set_random_id(self):
+        """Assign a newly-generated random query id to the message."""
+        self.set_id(dns.entropy.random_16())
+
     def use_edns(
         self,
         edns: int | bool | None = 0,
diff --git a/dns/query.py b/dns/query.py
index 5757d209..f668f493 100644
--- a/dns/query.py
+++ b/dns/query.py
@@ -681,7 +681,7 @@ def _http3(
     if url_parts.port is not None:
         port = url_parts.port
 
-    q.id = 0
+    q.set_id(0)
     wire = q.to_wire()
     the_connection: dns.quic.SyncQuicConnection
     the_manager: dns.quic.SyncQuicManager
@@ -1444,7 +1444,7 @@ def quic(
     if server_hostname is not None and hostname is None:
         hostname = server_hostname
 
-    q.id = 0
+    q.set_id(0)
     wire = q.to_wire()
     the_connection: dns.quic.SyncQuicConnection
     the_manager: dns.quic.SyncQuicManager
diff --git a/dns/resolver.py b/dns/resolver.py
index 6ded05ce..403c4222 100644
--- a/dns/resolver.py
+++ b/dns/resolver.py
@@ -32,7 +32,6 @@
 import dns._file_util
 import dns.edns
 import dns.exception
-import dns.flags
 import dns.inet
 import dns.ipv4
 import dns.ipv6
@@ -41,11 +40,9 @@
 import dns.nameserver
 import dns.query
 import dns.rcode
-import dns.rdata
 import dns.rdataclass
 import dns.rdatatype
 import dns.rdtypes.ANY.PTR
-import dns.rdtypes.svcbbase
 import dns.reversename
 import dns.tsig
 
@@ -1317,6 +1314,7 @@ def resolve(
                 nameserver, tcp, backoff = resolution.next_nameserver()
                 if backoff:
                     time.sleep(backoff)
+                request.set_random_id()
                 timeout = self._compute_timeout(start, lifetime, resolution.errors)
                 try:
                     response = nameserver.query(
diff --git a/doc/whatsnew.rst b/doc/whatsnew.rst
index b7aa190e..dd61953a 100644
--- a/doc/whatsnew.rst
+++ b/doc/whatsnew.rst
@@ -3,7 +3,7 @@
 What's New in dnspython
 =======================
 
-2.9.10 (in development)
+2.10.0 (in development)
 
 * The type annotation of ``public_key()`` on the ``dns.dnssecalgs`` private
   key classes is now ``dns.dnssecalgs.base.GenericPublicKey``, as declared by
@@ -18,6 +18,11 @@ What's New in dnspython
 2.9.1 (in development)
 ----------------------
 
+* The resolver now assigns a new random query id to every query.
+
+* For transports that require a 0 query id, set it in a way that does not break
+  TSIG.
+
 * ``dns.message.QueryMessage.resolve_chaining()`` now caps the minimum TTL of
   a negative response with no SOA record at 300 seconds
   (``dns.message.NEGATIVE_TTL_WITHOUT_SOA``).  Previously the TTL was left at
@@ -147,7 +152,7 @@ What's New in dnspython
   signed response failed with ``BadSignature`` and a response with no TSIG at
   all was accepted, as the RFC 8945 section 5.4 check for a missing TSIG was
   skipped.
-  
+
 * ``dns.query.inbound_xfr()``, ``dns.asyncquery.inbound_xfr()``, and
   ``dns.query.xfr()`` now check every response message with
   ``dns.message.Message.is_response()`` and raise ``dns.query.BadResponse`` if