diff --git a/src/core/net/dns_client.cpp b/src/core/net/dns_client.cpp
index 1b1b77ee5..49a0d4d5a 100644
--- a/src/core/net/dns_client.cpp
+++ b/src/core/net/dns_client.cpp
@@ -1520,7 +1520,17 @@ void Client::HandleTimer(void)
                     break;
                 }
 
-                IgnoreError(SendQuery(*query, info, /* aUpdateTimer */ false));
+#if OPENTHREAD_CONFIG_DNS_CLIENT_SERVICE_DISCOVERY_ENABLE
+                if (ReplaceWithSeparateSrvTxtQueries(*query) == kErrorNone)
+                {
+                    LogInfo("Switching to separate SRV/TXT on response timeout");
+                    info.ReadFrom(*query);
+                }
+                else
+#endif
+                {
+                    IgnoreError(SendQuery(*query, info, /* aUpdateTimer */ false));
+                }
             }
 
             nextTime.UpdateIfEarlier(info.mRetransmissionTime);
@@ -1534,7 +1544,7 @@ void Client::HandleTimer(void)
         }
     }
 
-    mTimer.FireAt(nextTime);
+    mTimer.FireAtIfEarlier(nextTime);
 
 #if OPENTHREAD_CONFIG_DNS_CLIENT_OVER_TCP_ENABLE
     if (!hasTcpQuery && mTcpState != kTcpUninitialized)
diff --git a/src/core/net/dnssd_server.cpp b/src/core/net/dnssd_server.cpp
index 7d512efc8..35c6cb793 100644
--- a/src/core/net/dnssd_server.cpp
+++ b/src/core/net/dnssd_server.cpp
@@ -163,7 +163,8 @@ exit:
 
 void Server::ProcessQuery(Request &aRequest)
 {
-    ResponseCode rcode = Header::kResponseSuccess;
+    ResponseCode rcode         = Header::kResponseSuccess;
+    bool         shouldRespond = true;
     Response     response(GetInstance());
 
 #if OPENTHREAD_CONFIG_DNS_UPSTREAM_QUERY_ENABLE
@@ -193,7 +194,7 @@ void Server::ProcessQuery(Request &aRequest)
     SuccessOrExit(rcode);
 #endif
 
-    SuccessOrExit(rcode = aRequest.ParseQuestions(mTestMode));
+    SuccessOrExit(rcode = aRequest.ParseQuestions(mTestMode, shouldRespond));
     SuccessOrExit(rcode = response.AddQuestionsFrom(aRequest));
 
 #if OT_SHOULD_LOG_AT(OT_LOG_LEVEL_INFO)
@@ -225,7 +226,10 @@ exit:
         response.SetResponseCode(rcode);
     }
 
-    response.Send(*aRequest.mMessageInfo);
+    if (shouldRespond)
+    {
+        response.Send(*aRequest.mMessageInfo);
+    }
 }
 
 Server::Response::Response(Instance &aInstance)
@@ -296,7 +300,7 @@ exit:
     return;
 }
 
-Server::ResponseCode Server::Request::ParseQuestions(uint8_t aTestMode)
+Server::ResponseCode Server::Request::ParseQuestions(uint8_t aTestMode, bool &aShouldRespond)
 {
     // Parse header and questions from a `Request` query message and
     // determine the `QueryType`.
@@ -306,6 +310,8 @@ Server::ResponseCode Server::Request::ParseQuestions(uint8_t aTestMode)
     uint16_t     questionCount = mHeader.GetQuestionCount();
     Question     question;
 
+    aShouldRespond = true;
+
     VerifyOrExit(mHeader.GetQueryType() == Header::kQueryTypeStandard, rcode = Header::kResponseNotImplemented);
     VerifyOrExit(!mHeader.IsTruncationFlagSet());
 
@@ -335,7 +341,8 @@ Server::ResponseCode Server::Request::ParseQuestions(uint8_t aTestMode)
 
     if (questionCount > 1)
     {
-        VerifyOrExit(!(aTestMode & kTestModeSingleQuestionOnly));
+        VerifyOrExit(!(aTestMode & kTestModeRejectMultiQuestionQuery));
+        VerifyOrExit(!(aTestMode & kTestModeIgnoreMultiQuestionQuery), aShouldRespond = false);
 
         VerifyOrExit(questionCount == 2);
 
diff --git a/src/core/net/dnssd_server.hpp b/src/core/net/dnssd_server.hpp
index ea8f7e7d7..f584e3b12 100644
--- a/src/core/net/dnssd_server.hpp
+++ b/src/core/net/dnssd_server.hpp
@@ -291,8 +291,9 @@ public:
      */
     enum TestModeFlags : uint8_t
     {
-        kTestModeSingleQuestionOnly     = 1 << 0, ///< Allow single question in query, send `FormatError` otherwise.
-        kTestModeEmptyAdditionalSection = 1 << 1, ///< Do not include any RR in additional section.
+        kTestModeRejectMultiQuestionQuery = 1 << 0, ///< Send `FormatError` for a query with multiple questions.
+        kTestModeIgnoreMultiQuestionQuery = 1 << 1, ///< Ignore a query with multiple questions (send no response).
+        kTestModeEmptyAdditionalSection   = 1 << 2, ///< Do not include any RR in additional section.
     };
 
     static constexpr uint8_t kTestModeDisabled = 0; ///< Test mode is disabled (no flags).
@@ -346,7 +347,7 @@ private:
 
     struct Request
     {
-        ResponseCode ParseQuestions(uint8_t aTestMode);
+        ResponseCode ParseQuestions(uint8_t aTestMode, bool &aShouldRespond);
 
         const Message          *mMessage;
         const Ip6::MessageInfo *mMessageInfo;
diff --git a/tests/unit/test_dns_client.cpp b/tests/unit/test_dns_client.cpp
index 176654c0f..e91376689 100644
--- a/tests/unit/test_dns_client.cpp
+++ b/tests/unit/test_dns_client.cpp
@@ -671,8 +671,8 @@ void TestDnsClient(void)
 
     Log("- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - ");
 
-    Log("Set TestMode on server to only accept single question");
-    dnsServer->SetTestMode(Dns::ServiceDiscovery::Server::kTestModeSingleQuestionOnly);
+    Log("Set TestMode on server to reject multi-question queries and send error");
+    dnsServer->SetTestMode(Dns::ServiceDiscovery::Server::kTestModeRejectMultiQuestionQuery);
 
     Log("ResolveService(%s,%s) with ServiceMode %s", kInstance1Label, kService1FullName,
         ServiceModeToString(Dns::Client::QueryConfig::kServiceModeSrvTxtOptimize));
@@ -706,6 +706,48 @@ void TestDnsClient(void)
 
     dnsServer->SetTestMode(Dns::ServiceDiscovery::Server::kTestModeDisabled);
 
+    Log("- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - ");
+
+    Log("Set TestMode on server to ignore multi-question queries (send no response)");
+    dnsServer->SetTestMode(Dns::ServiceDiscovery::Server::kTestModeIgnoreMultiQuestionQuery);
+
+    Log("ResolveService(%s,%s) with ServiceMode %s", kInstance1Label, kService1FullName,
+        ServiceModeToString(Dns::Client::QueryConfig::kServiceModeSrvTxtOptimize));
+
+    queryConfig.Clear();
+    queryConfig.mServiceMode = static_cast<otDnsServiceMode>(Dns::Client::QueryConfig::kServiceModeSrvTxtOptimize);
+
+    sResolveServiceInfo.Reset();
+    SuccessOrQuit(
+        dnsClient->ResolveService(kInstance1Label, kService1FullName, ServiceCallback, sInstance, &queryConfig));
+
+    AdvanceTime(10 * 1000); // Wait longer than client response timeout.
+
+    VerifyOrQuit(sResolveServiceInfo.mCallbackCount == 1);
+    SuccessOrQuit(sResolveServiceInfo.mError);
+
+    // Use `kServiceModeSrvTxt` and check that server does ignore two questions.
+
+    Log("ResolveService(%s,%s) with ServiceMode %s", kInstance1Label, kService1FullName,
+        ServiceModeToString(Dns::Client::QueryConfig::kServiceModeSrvTxt));
+
+    queryConfig.Clear();
+    queryConfig.mServiceMode = static_cast<otDnsServiceMode>(Dns::Client::QueryConfig::kServiceModeSrvTxt);
+
+    sResolveServiceInfo.Reset();
+    SuccessOrQuit(
+        dnsClient->ResolveService(kInstance1Label, kService1FullName, ServiceCallback, sInstance, &queryConfig));
+
+    // Wait for the client to time out after exhausting all retry attempts, and
+    // ensure that a `kErrorResponseTimeout` error is reported.
+
+    AdvanceTime(45 * 1000);
+
+    VerifyOrQuit(sResolveServiceInfo.mCallbackCount == 1);
+    VerifyOrQuit(sResolveServiceInfo.mError == kErrorResponseTimeout);
+
+    dnsServer->SetTestMode(Dns::ServiceDiscovery::Server::kTestModeDisabled);
+
     //- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -
     // Validate DNS Client `ResolveService()` using all service modes
     // when sever does not provide any RR in the addition data section.
@@ -832,7 +874,7 @@ void TestDnsClient(void)
     Log("- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - ");
     Log("Set TestMode on server to not include any RR in additional section AND to only accept single question");
     dnsServer->SetTestMode(Dns::ServiceDiscovery::Server::kTestModeEmptyAdditionalSection +
-                           Dns::ServiceDiscovery::Server::kTestModeSingleQuestionOnly);
+                           Dns::ServiceDiscovery::Server::kTestModeRejectMultiQuestionQuery);
 
     Log("ResolveServiceAndHostAddress(%s,%s) with ServiceMode: %s", kInstance1Label, kService1FullName,
         ServiceModeToString(Dns::Client::QueryConfig::kServiceModeSrvTxtOptimize));