diff --git a/images/router/haproxy/conf/haproxy-config.template b/images/router/haproxy/conf/haproxy-config.template
index 797db3226..3c7e9e245 100644
--- a/images/router/haproxy/conf/haproxy-config.template
+++ b/images/router/haproxy/conf/haproxy-config.template
@@ -158,14 +158,10 @@ defaults
   timeout connect {{ firstMatch $timeSpecPattern (env "ROUTER_DEFAULT_CONNECT_TIMEOUT") "5s" }}
   timeout client {{ firstMatch $timeSpecPattern (env "ROUTER_DEFAULT_CLIENT_TIMEOUT") "30s" }}
   timeout client-fin {{ firstMatch $timeSpecPattern (env "ROUTER_CLIENT_FIN_TIMEOUT") "1s" }}
-  timeout server {{ firstMatch $timeSpecPattern (env "ROUTER_DEFAULT_SERVER_TIMEOUT") "30s" }}
   timeout server-fin {{ firstMatch $timeSpecPattern (env "ROUTER_DEFAULT_SERVER_FIN_TIMEOUT") "1s" }}
   timeout http-request {{ firstMatch $timeSpecPattern (env "ROUTER_SLOWLORIS_TIMEOUT") "10s" }}
   timeout http-keep-alive {{ firstMatch $timeSpecPattern (env "ROUTER_SLOWLORIS_HTTP_KEEPALIVE") "300s" }}
 
-  # Long timeout for WebSocket connections.
-  timeout tunnel {{ firstMatch $timeSpecPattern (env "ROUTER_DEFAULT_TUNNEL_TIMEOUT") "1h" }}
-
   {{- if isTrue (env "ROUTER_ENABLE_COMPRESSION") }}
   compression algo gzip
   compression type {{ env "ROUTER_COMPRESSION_MIME" "text/html text/plain text/css" }}
@@ -312,6 +308,9 @@ frontend public_ssl
 # traffic
 ##########################################################################
 backend be_sni
+        {{- with $value := maxTimeoutFirstMatchedAndClipped .State "haproxy.router.openshift.io/timeout" $timeSpecPattern (env "ROUTER_DEFAULT_SERVER_TIMEOUT") "30s"  }}
+  timeout server  {{ $value }}
+        {{- end }}
   server fe_sni unix@/var/lib/haproxy/run/haproxy-sni.sock weight 1 send-proxy
 
 frontend fe_sni
@@ -425,6 +424,9 @@ frontend fe_sni
 ##########################################################################
 # backend for when sni does not exist, or ssl term needs to happen on the edge
 backend be_no_sni
+        {{- with $value := maxTimeoutFirstMatchedAndClipped .State "haproxy.router.openshift.io/timeout" $timeSpecPattern (env "ROUTER_DEFAULT_SERVER_TIMEOUT") "30s"  }}
+  timeout server  {{ $value }}
+        {{- end }}
   server fe_no_sni unix@/var/lib/haproxy/run/haproxy-no-sni.sock weight 1 send-proxy
 
 frontend fe_no_sni
@@ -581,10 +583,10 @@ backend {{ genBackendNamePrefix $cfg.TLSTermination }}:{{ $cfgIdx }}
           {{- end }}
   tcp-request content reject if !whitelist
         {{- end }}
-        {{- with $value := clipHAProxyTimeoutValue (firstMatch $timeSpecPattern (index $cfg.Annotations "haproxy.router.openshift.io/timeout")) }}
+        {{- with $value := clipHAProxyTimeoutValue (firstMatch $timeSpecPattern (index $cfg.Annotations "haproxy.router.openshift.io/timeout") (env "ROUTER_DEFAULT_SERVER_TIMEOUT") "30s") }}
   timeout server  {{ $value }}
         {{- end }}
-        {{- with $value := clipHAProxyTimeoutValue (firstMatch $timeSpecPattern (index $cfg.Annotations "haproxy.router.openshift.io/timeout-tunnel")) }}
+        {{- with $value := clipHAProxyTimeoutValue (firstMatch $timeSpecPattern (index $cfg.Annotations "haproxy.router.openshift.io/timeout-tunnel") (env "ROUTER_DEFAULT_TUNNEL_TIMEOUT") "1h") }}
   timeout tunnel  {{ $value }}
         {{- end }}
 
@@ -785,7 +787,10 @@ backend {{ genBackendNamePrefix $cfg.TLSTermination }}:{{ $cfgIdx }}
           {{- end }}
   tcp-request content reject if !whitelist
         {{- end }}
-        {{- with $value := clipHAProxyTimeoutValue (firstMatch $timeSpecPattern (index $cfg.Annotations "haproxy.router.openshift.io/timeout-tunnel") (index $cfg.Annotations "haproxy.router.openshift.io/timeout")) }}
+        {{- with $value := clipHAProxyTimeoutValue (firstMatch $timeSpecPattern (index $cfg.Annotations "haproxy.router.openshift.io/timeout") (env "ROUTER_DEFAULT_SERVER_TIMEOUT") "30s") }}
+  timeout server  {{ $value }}
+        {{- end }}
+        {{- with $value := clipHAProxyTimeoutValue (firstMatch $timeSpecPattern (index $cfg.Annotations "haproxy.router.openshift.io/timeout-tunnel") (index $cfg.Annotations "haproxy.router.openshift.io/timeout") (env "ROUTER_DEFAULT_TUNNEL_TIMEOUT") "1h") }}
   timeout tunnel  {{ $value }}
         {{- end }}
 
diff --git a/pkg/router/template/template_helper.go b/pkg/router/template/template_helper.go
index 7ce99c22c..7ede52d26 100644
--- a/pkg/router/template/template_helper.go
+++ b/pkg/router/template/template_helper.go
@@ -13,6 +13,7 @@ import (
 	"strings"
 	"sync"
 	"text/template"
+	"time"
 
 	routev1 "github.com/openshift/api/route/v1"
 	"github.com/openshift/router/pkg/router/routeapihelpers"
@@ -386,6 +387,27 @@ func parseIPList(list string) string {
 	return list
 }
 
+// maxTimeoutFirstMatchedAndClipped finds the maximum timeout managed by a given annotation among all the routes, matches it against a given pattern, and clips.
+func maxTimeoutFirstMatchedAndClipped(aliases map[ServiceAliasConfigKey]ServiceAliasConfig, annotation, pattern string, values ...string) string {
+	var (
+		max         string
+		maxDuration time.Duration
+	)
+	for _, cfg := range aliases {
+		timeout := clipHAProxyTimeoutValue(firstMatch(pattern, append([]string{cfg.Annotations[annotation]}, values...)...))
+		if timeout != "" {
+			// No error handling because clipHAProxyTimeoutValue returns
+			// a valid timeout or an empty string. The latter is already handled.
+			timeoutDuration, _ := time.ParseDuration(timeout)
+			if timeoutDuration > maxDuration {
+				max = timeout
+				maxDuration = timeoutDuration
+			}
+		}
+	}
+	return max
+}
+
 var helperFunctions = template.FuncMap{
 	"endpointsForAlias":        endpointsForAlias,        //returns the list of valid endpoints
 	"processEndpointsForAlias": processEndpointsForAlias, //returns the list of valid endpoints after processing them
@@ -409,6 +431,7 @@ var helperFunctions = template.FuncMap{
 	"validateHAProxyWhiteList":     validateHAProxyWhiteList,     //validates a haproxy whitelist (acl) content
 	"generateHAProxyWhiteListFile": generateHAProxyWhiteListFile, //generates a haproxy whitelist file for use in an acl
 
-	"clipHAProxyTimeoutValue": clipHAProxyTimeoutValue, //clips extrodinarily high timeout values to be below the maximum allowed timeout value
-	"parseIPList":             parseIPList,             //parses the list of IPs/CIDRs (IPv4/IPv6)
+	"clipHAProxyTimeoutValue":          clipHAProxyTimeoutValue,          //clips extraordinarily high timeout values to be below the maximum allowed timeout value
+	"parseIPList":                      parseIPList,                      //parses the list of IPs/CIDRs (IPv4/IPv6)
+	"maxTimeoutFirstMatchedAndClipped": maxTimeoutFirstMatchedAndClipped, //finds the maximum timeout managed by a given annotation among all the routes, matches it against a given pattern, and clips
 }
diff --git a/pkg/router/template/template_helper_test.go b/pkg/router/template/template_helper_test.go
index 03b1177bc..300ee3eb9 100644
--- a/pkg/router/template/template_helper_test.go
+++ b/pkg/router/template/template_helper_test.go
@@ -1067,3 +1067,105 @@ func TestParseIPList(t *testing.T) {
 		})
 	}
 }
+
+func TestMaxTimeoutFirstMatchedAndClipped(t *testing.T) {
+	testCases := []struct {
+		name       string
+		state      map[ServiceAliasConfigKey]ServiceAliasConfig
+		annotation string
+		pattern    string
+		values     []string
+		expected   string
+	}{
+		{
+			name: "Route timeout is maximum",
+			state: map[ServiceAliasConfigKey]ServiceAliasConfig{
+				"test:route1": {
+					Annotations: map[string]string{
+						"haproxy.router.openshift.io/timeout": "5m",
+					},
+				},
+				"test:route2": {
+					Annotations: map[string]string{
+						"haproxy.router.openshift.io/timeout": "35s",
+					},
+				},
+				"test:route3": {
+					Annotations: map[string]string{
+						"haproxy.router.openshift.io/timeout-tunnel": "10m",
+					},
+				},
+				"test:route4": {},
+			},
+			annotation: "haproxy.router.openshift.io/timeout",
+			pattern:    `[1-9][0-9]*(us|ms|s|m|h|d)?`,
+			values:     []string{"30s"},
+			expected:   "5m",
+		},
+		{
+			name: "Default timeout is maximum",
+			state: map[ServiceAliasConfigKey]ServiceAliasConfig{
+				"test:route1": {},
+				"test:route2": {},
+				"test:route3": {},
+			},
+			annotation: "haproxy.router.openshift.io/timeout",
+			pattern:    `[1-9][0-9]*(us|ms|s|m|h|d)?`,
+			values:     []string{"30s"},
+			expected:   "30s",
+		},
+		{
+			name: "Maximum default timeout is choosen",
+			state: map[ServiceAliasConfigKey]ServiceAliasConfig{
+				"test:route1": {},
+				"test:route2": {},
+				"test:route3": {},
+			},
+			annotation: "haproxy.router.openshift.io/timeout",
+			pattern:    `[1-9][0-9]*(us|ms|s|m|h|d)?`,
+			values:     []string{"40s", "30s"},
+			expected:   "40s",
+		},
+		{
+			name: "Route timeout doesn't match",
+			state: map[ServiceAliasConfigKey]ServiceAliasConfig{
+				"test:route1": {
+					Annotations: map[string]string{
+						"haproxy.router.openshift.io/timeout": "5minutes",
+					},
+				},
+				"test:route2": {
+					Annotations: map[string]string{
+						"haproxy.router.openshift.io/timeout": "35s",
+					},
+				},
+			},
+			annotation: "haproxy.router.openshift.io/timeout",
+			pattern:    `[1-9][0-9]*(us|ms|s|m|h|d)?`,
+			values:     []string{"30s"},
+			expected:   "35s",
+		},
+		{
+			name: "Route timeout clipped",
+			state: map[ServiceAliasConfigKey]ServiceAliasConfig{
+				"test:route1": {
+					Annotations: map[string]string{
+						"haproxy.router.openshift.io/timeout": "999999999s",
+					},
+				},
+			},
+			annotation: "haproxy.router.openshift.io/timeout",
+			pattern:    `[1-9][0-9]*(us|ms|s|m|h|d)?`,
+			values:     []string{"30s"},
+			expected:   "2147483647ms",
+		},
+	}
+	for _, tc := range testCases {
+		t.Run(tc.name, func(t *testing.T) {
+			got := maxTimeoutFirstMatchedAndClipped(tc.state, tc.annotation, tc.pattern, tc.values...)
+			if got != tc.expected {
+				t.Errorf("Failure: expected %q, got %q", tc.expected, got)
+			}
+		})
+	}
+}