diff --git a/chart/templates/_helpers.yaml b/chart/templates/_helpers.yaml
index 2100e2d4267f2..8838b837dca0f 100644
--- a/chart/templates/_helpers.yaml
+++ b/chart/templates/_helpers.yaml
@@ -91,13 +91,20 @@ If release name contains chart name it will be used as a full name.
         name: {{ template "airflow_metadata_secret" . }}
         key: kedaConnection
   {{- end }}
-  {{- if .Values.enableBuiltInSecretEnvVars.AIRFLOW__WEBSERVER__SECRET_KEY }}
+  {{- if and (semverCompare "<3.0.0" .Values.airflowVersion) .Values.enableBuiltInSecretEnvVars.AIRFLOW__WEBSERVER__SECRET_KEY }}
   - name: AIRFLOW__WEBSERVER__SECRET_KEY
     valueFrom:
       secretKeyRef:
         name: {{ template "webserver_secret_key_secret" . }}
         key: webserver-secret-key
   {{- end }}
+  {{- if and (semverCompare ">=3.0.0" .Values.airflowVersion) .Values.enableBuiltInSecretEnvVars.AIRFLOW__API__SECRET_KEY }}
+  - name: AIRFLOW__API__SECRET_KEY
+    valueFrom:
+      secretKeyRef:
+        name: {{ template "api_secret_key_secret" . }}
+        key: api-secret-key
+  {{- end }}
   {{- if and (semverCompare ">=3.0.0" .Values.airflowVersion) .Values.enableBuiltInSecretEnvVars.AIRFLOW__API_AUTH__JWT_SECRET }}
   - name: AIRFLOW__API_AUTH__JWT_SECRET
     valueFrom:
@@ -411,6 +418,10 @@ If release name contains chart name it will be used as a full name.
   {{- default (printf "%s-webserver-secret-key" (include "airflow.fullname" .)) .Values.webserverSecretKeySecretName }}
 {{- end }}
 
+{{- define "api_secret_key_secret" -}}
+  {{- default (printf "%s-api-secret-key" (include "airflow.fullname" .)) .Values.apiSecretKeySecretName }}
+{{- end }}
+
 {{- define "redis_password_secret" -}}
   {{- default (printf "%s-redis-password" .Release.Name) .Values.redis.passwordSecretName }}
 {{- end }}
diff --git a/chart/templates/secrets/api-secret-key-secret.yaml b/chart/templates/secrets/api-secret-key-secret.yaml
new file mode 100644
index 0000000000000..52e0fff689f44
--- /dev/null
+++ b/chart/templates/secrets/api-secret-key-secret.yaml
@@ -0,0 +1,44 @@
+{{/*
+ Licensed to the Apache Software Foundation (ASF) under one
+ or more contributor license agreements.  See the NOTICE file
+ distributed with this work for additional information
+ regarding copyright ownership.  The ASF licenses this file
+ to you under the Apache License, Version 2.0 (the
+ "License"); you may not use this file except in compliance
+ with the License.  You may obtain a copy of the License at
+
+   http://www.apache.org/licenses/LICENSE-2.0
+
+ Unless required by applicable law or agreed to in writing,
+ software distributed under the License is distributed on an
+ "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
+ KIND, either express or implied.  See the License for the
+ specific language governing permissions and limitations
+ under the License.
+*/}}
+
+############################################
+## Airflow Api Flask Secret Key Secret
+############################################
+{{- if and (semverCompare ">=3.0.0" .Values.airflowVersion) (not .Values.apiSecretKeySecretName) }}
+apiVersion: v1
+kind: Secret
+metadata:
+  name: {{ include "airflow.fullname" . }}-api-secret-key
+  labels:
+    tier: airflow
+    component: api-server
+    release: {{ .Release.Name }}
+    chart: "{{ .Chart.Name }}-{{ .Chart.Version }}"
+    heritage: {{ .Release.Service }}
+    {{- with .Values.labels }}
+      {{- toYaml . | nindent 4 }}
+    {{- end }}
+  {{- with .Values.apiSecretAnnotations }}
+  annotations:
+    {{- toYaml . | nindent 4 }}
+  {{- end }}
+type: Opaque
+data:
+  api-secret-key: {{ (.Values.apiSecretKey) | default (randAlphaNum 32) | b64enc | quote }}
+{{- end }}
diff --git a/chart/templates/secrets/fernetkey-secret.yaml b/chart/templates/secrets/fernetkey-secret.yaml
index 5461b56f03c28..a9a1f6016938b 100644
--- a/chart/templates/secrets/fernetkey-secret.yaml
+++ b/chart/templates/secrets/fernetkey-secret.yaml
@@ -21,7 +21,6 @@
 ## Airflow Fernet Key Secret
 #################################
 {{- if not .Values.fernetKeySecretName }}
-{{- $generated_fernet_key := (randAlphaNum 32 | b64enc) }}
 apiVersion: v1
 kind: Secret
 metadata:
@@ -43,5 +42,5 @@ metadata:
     {{- end }}
 type: Opaque
 data:
-  fernet-key: {{ (default $generated_fernet_key .Values.fernetKey) | b64enc | quote }}
+  fernet-key: {{ (.Values.fernetKey) | default (randAlphaNum 32) | b64enc | quote }}
 {{- end }}
diff --git a/chart/templates/secrets/webserver-secret-key-secret.yaml b/chart/templates/secrets/webserver-secret-key-secret.yaml
index 5a9025236e7af..e7803c4d84033 100644
--- a/chart/templates/secrets/webserver-secret-key-secret.yaml
+++ b/chart/templates/secrets/webserver-secret-key-secret.yaml
@@ -20,8 +20,7 @@
 ############################################
 ## Airflow Webserver Flask Secret Key Secret
 ############################################
-{{- if not .Values.webserverSecretKeySecretName }}
-{{ $generated_secret_key := (randAlphaNum 32 | b64enc) }}
+{{- if and (semverCompare "<3.0.0" .Values.airflowVersion) .Values.webserver.enabled (not .Values.webserverSecretKeySecretName) }}
 apiVersion: v1
 kind: Secret
 metadata:
@@ -41,5 +40,5 @@ metadata:
   {{- end }}
 type: Opaque
 data:
-  webserver-secret-key: {{ (default $generated_secret_key .Values.webserverSecretKey) | b64enc | quote }}
+  webserver-secret-key: {{ (.Values.webserverSecretKey) | default (randAlphaNum 32) | b64enc | quote }}
 {{- end }}
diff --git a/chart/values.schema.json b/chart/values.schema.json
index 1bfe3c9757b69..b329b4a0dde76 100644
--- a/chart/values.schema.json
+++ b/chart/values.schema.json
@@ -1064,6 +1064,11 @@
                     "type": "boolean",
                     "default": true
                 },
+                "AIRFLOW__API__SECRET_KEY": {
+                    "description": "Enable ``AIRFLOW__API__SECRET_KEY`` variable to be read from the Api Secret Key Secret",
+                    "type": "boolean",
+                    "default": true
+                },
                 "AIRFLOW__API_AUTH__JWT_SECRET": {
                     "description": "Enable ``AIRFLOW__API_AUTH__JWT_SECRET`` variable to be read from the JWT Secret",
                     "type": "boolean",
@@ -1464,6 +1469,33 @@
                 "type": "string"
             }
         },
+        "apiSecretKey": {
+            "description": "The Flask secret key for Airflow Api to encrypt browser session.",
+            "type": [
+                "string",
+                "null"
+            ],
+            "x-docsSection": "Common",
+            "default": null
+        },
+        "apiSecretAnnotations": {
+            "description": "Annotations to add to the Api secret.",
+            "type": "object",
+            "x-docsSection": "Common",
+            "default": {},
+            "additionalProperties": {
+                "type": "string"
+            }
+        },
+        "apiSecretKeySecretName": {
+            "description": "The Secret name containing Flask secret_key for the Api.",
+            "type": [
+                "string",
+                "null"
+            ],
+            "x-docsSection": "Airflow",
+            "default": null
+        },
         "jwtSecret": {
             "description": "Secret key used to encode and decode JWTs to authenticate to public and private APIs (can only be set during install, not upgrade).",
             "type": [
diff --git a/chart/values.yaml b/chart/values.yaml
index 5d85210d419f1..cff157e6d50ae 100644
--- a/chart/values.yaml
+++ b/chart/values.yaml
@@ -407,6 +407,7 @@ enableBuiltInSecretEnvVars:
   AIRFLOW__CORE__SQL_ALCHEMY_CONN: true
   AIRFLOW__DATABASE__SQL_ALCHEMY_CONN: true
   AIRFLOW_CONN_AIRFLOW_DB: true
+  AIRFLOW__API__SECRET_KEY: true
   AIRFLOW__API_AUTH__JWT_SECRET: true
   AIRFLOW__WEBSERVER__SECRET_KEY: true
   AIRFLOW__CELERY__CELERY_RESULT_BACKEND: true
@@ -551,11 +552,11 @@ fernetKeySecretName: ~
 # Add custom annotations to the fernet key secret
 fernetKeySecretAnnotations: {}
 
-# Flask secret key for Airflow Webserver: `[webserver] secret_key` in airflow.cfg
-webserverSecretKey: ~
-# Add custom annotations to the webserver secret
-webserverSecretAnnotations: {}
-webserverSecretKeySecretName: ~
+# Flask secret key for Airflow 3+ Api: `[api] secret_key` in airflow.cfg
+apiSecretKey: ~
+# Add custom annotations to the api secret
+apiSecretAnnotations: {}
+apiSecretKeySecretName: ~
 
 # Secret key used to encode and decode JWTs: `[api_auth] jwt_secret` in airflow.cfg
 jwtSecret: ~
@@ -563,6 +564,12 @@ jwtSecret: ~
 jwtSecretAnnotations: {}
 jwtSecretName: ~
 
+# Flask secret key for Airflow <3 Webserver: `[webserver] secret_key` in airflow.cfg
+webserverSecretKey: ~
+# Add custom annotations to the webserver secret
+webserverSecretAnnotations: {}
+webserverSecretKeySecretName: ~
+
 # In order to use kerberos you need to create secret containing the keytab file
 # The secret name should follow naming convention of the application where resources are
 # name {{ .Release-name }}-<POSTFIX>. In case of the keytab file, the postfix is "kerberos-keytab"
diff --git a/helm-tests/tests/helm_tests/airflow_aux/test_airflow_common.py b/helm-tests/tests/helm_tests/airflow_aux/test_airflow_common.py
index e6b247afb1cd0..f4ad5b6e170e3 100644
--- a/helm-tests/tests/helm_tests/airflow_aux/test_airflow_common.py
+++ b/helm-tests/tests/helm_tests/airflow_aux/test_airflow_common.py
@@ -323,6 +323,7 @@ def test_should_disable_some_variables(self):
                 "enableBuiltInSecretEnvVars": {
                     "AIRFLOW__CORE__SQL_ALCHEMY_CONN": False,
                     "AIRFLOW__DATABASE__SQL_ALCHEMY_CONN": False,
+                    "AIRFLOW__API__SECRET_KEY": False,
                     "AIRFLOW__API_AUTH__JWT_SECRET": False,
                     "AIRFLOW__WEBSERVER__SECRET_KEY": False,
                     # the following vars only appear if remote logging is set, so disabling them in this test is kind of a no-op
@@ -370,7 +371,7 @@ def test_have_all_variables(self):
             "AIRFLOW__CORE__SQL_ALCHEMY_CONN",
             "AIRFLOW__DATABASE__SQL_ALCHEMY_CONN",
             "AIRFLOW_CONN_AIRFLOW_DB",
-            "AIRFLOW__WEBSERVER__SECRET_KEY",
+            "AIRFLOW__API__SECRET_KEY",
             "AIRFLOW__API_AUTH__JWT_SECRET",
             "AIRFLOW__CELERY__BROKER_URL",
         ]
diff --git a/helm-tests/tests/helm_tests/airflow_aux/test_basic_helm_chart.py b/helm-tests/tests/helm_tests/airflow_aux/test_basic_helm_chart.py
index a3cc64b96688e..46f617943a884 100644
--- a/helm-tests/tests/helm_tests/airflow_aux/test_basic_helm_chart.py
+++ b/helm-tests/tests/helm_tests/airflow_aux/test_basic_helm_chart.py
@@ -38,7 +38,6 @@
     ("Secret", "test-basic-airflow-metadata"),
     ("Secret", "test-basic-broker-url"),
     ("Secret", "test-basic-fernet-key"),
-    ("Secret", "test-basic-airflow-webserver-secret-key"),
     ("Secret", "test-basic-redis-password"),
     ("Secret", "test-basic-postgresql"),
     ("ConfigMap", "test-basic-airflow-config"),
@@ -71,6 +70,7 @@
         ("Deployment", "test-basic-airflow-dag-processor"),
         ("ServiceAccount", "test-basic-airflow-api-server"),
         ("ServiceAccount", "test-basic-airflow-dag-processor"),
+        ("Secret", "test-basic-airflow-api-secret-key"),
         ("Secret", "test-basic-jwt-secret"),
     }
 )
@@ -82,6 +82,7 @@
         ("Service", "test-basic-airflow-webserver"),
         ("Deployment", "test-basic-airflow-webserver"),
         ("ServiceAccount", "test-basic-airflow-webserver"),
+        ("Secret", "test-basic-airflow-webserver-secret-key"),
     }
 )
 
@@ -137,7 +138,6 @@ def test_basic_deployments(self, version):
             ("Secret", "test-basic-metadata"),
             ("Secret", "test-basic-broker-url"),
             ("Secret", "test-basic-fernet-key"),
-            ("Secret", "test-basic-webserver-secret-key"),
             ("Secret", "test-basic-postgresql"),
             ("Secret", "test-basic-redis-password"),
             ("ConfigMap", "test-basic-config"),
@@ -171,6 +171,7 @@ def test_basic_deployments(self, version):
                     ("ServiceAccount", "test-basic-api-server"),
                     ("ServiceAccount", "test-basic-dag-processor"),
                     ("Service", "test-basic-triggerer"),
+                    ("Secret", "test-basic-api-secret-key"),
                     ("Secret", "test-basic-jwt-secret"),
                 )
             )
@@ -180,6 +181,7 @@ def test_basic_deployments(self, version):
                     ("Deployment", "test-basic-webserver"),
                     ("Service", "test-basic-webserver"),
                     ("ServiceAccount", "test-basic-webserver"),
+                    ("Secret", "test-basic-webserver-secret-key"),
                 )
             )
         if version == "default":
@@ -238,7 +240,6 @@ def test_basic_deployment_with_standalone_dag_processor(self, version):
             ("Secret", "test-basic-metadata"),
             ("Secret", "test-basic-broker-url"),
             ("Secret", "test-basic-fernet-key"),
-            ("Secret", "test-basic-webserver-secret-key"),
             ("Secret", "test-basic-postgresql"),
             ("Secret", "test-basic-redis-password"),
             ("ConfigMap", "test-basic-config"),
@@ -271,6 +272,7 @@ def test_basic_deployment_with_standalone_dag_processor(self, version):
                     ("Deployment", "test-basic-api-server"),
                     ("Service", "test-basic-api-server"),
                     ("ServiceAccount", "test-basic-api-server"),
+                    ("Secret", "test-basic-api-secret-key"),
                     ("Secret", "test-basic-jwt-secret"),
                 }
             )
@@ -280,6 +282,7 @@ def test_basic_deployment_with_standalone_dag_processor(self, version):
                     ("Service", "test-basic-webserver"),
                     ("Deployment", "test-basic-webserver"),
                     ("ServiceAccount", "test-basic-webserver"),
+                    ("Secret", "test-basic-webserver-secret-key"),
                 }
             )
         assert list_of_kind_names_tuples == expected
@@ -447,7 +450,6 @@ def test_labels_are_valid(self, airflow_version):
             (f"{release_name}-statsd", "Deployment", "statsd"),
             (f"{release_name}-statsd", "Service", "statsd"),
             (f"{release_name}-statsd-policy", "NetworkPolicy", "statsd-policy"),
-            (f"{release_name}-webserver-secret-key", "Secret", "webserver"),
             (f"{release_name}-worker", "Service", "worker"),
             (f"{release_name}-worker", "StatefulSet", "worker"),
             (f"{release_name}-worker-policy", "NetworkPolicy", "airflow-worker-policy"),
@@ -460,14 +462,17 @@ def test_labels_are_valid(self, airflow_version):
         if self._is_airflow_3_or_above(airflow_version):
             kind_names_tuples += [
                 (f"{release_name}-api-server", "Service", "api-server"),
-                (f"{release_name}-api-server-policy", "NetworkPolicy", "airflow-api-server-policy"),
                 (f"{release_name}-api-server", "Deployment", "api-server"),
+                (f"{release_name}-airflow-api-server", "ServiceAccount", "api-server"),
+                (f"{release_name}-api-secret-key", "Secret", "api-server"),
+                (f"{release_name}-api-server-policy", "NetworkPolicy", "airflow-api-server-policy"),
             ]
         else:
             kind_names_tuples += [
                 (f"{release_name}-airflow-webserver", "ServiceAccount", "webserver"),
                 (f"{release_name}-webserver", "Deployment", "webserver"),
                 (f"{release_name}-webserver", "Service", "webserver"),
+                (f"{release_name}-webserver-secret-key", "Secret", "webserver"),
                 (f"{release_name}-webserver-policy", "NetworkPolicy", "airflow-webserver-policy"),
                 (f"{release_name}-ingress", "Ingress", "airflow-ingress"),
             ]
diff --git a/helm-tests/tests/helm_tests/apiserver/test_apiserver.py b/helm-tests/tests/helm_tests/apiserver/test_apiserver.py
index 08796bde0c855..2db007234fed1 100644
--- a/helm-tests/tests/helm_tests/apiserver/test_apiserver.py
+++ b/helm-tests/tests/helm_tests/apiserver/test_apiserver.py
@@ -90,3 +90,19 @@ def test_should_add_annotations_to_jwt_secret(self):
 
         assert "annotations" in jmespath.search("metadata", docs)
         assert jmespath.search("metadata.annotations", docs)["test_annotation"] == "test_annotation_value"
+
+
+class TestApiSecretKeySecret:
+    """Tests api secret key secret."""
+
+    def test_should_add_annotations_to_api_secret_key_secret(self):
+        docs = render_chart(
+            values={
+                "airflowVersion": "3.0.0",
+                "apiSecretAnnotations": {"test_annotation": "test_annotation_value"},
+            },
+            show_only=["templates/secrets/api-secret-key-secret.yaml"],
+        )[0]
+
+        assert "annotations" in jmespath.search("metadata", docs)
+        assert jmespath.search("metadata.annotations", docs)["test_annotation"] == "test_annotation_value"
diff --git a/helm-tests/tests/helm_tests/security/test_rbac.py b/helm-tests/tests/helm_tests/security/test_rbac.py
index 3a4476644409a..aa93a91b691fe 100644
--- a/helm-tests/tests/helm_tests/security/test_rbac.py
+++ b/helm-tests/tests/helm_tests/security/test_rbac.py
@@ -47,7 +47,6 @@
     ("Secret", "test-rbac-broker-url"),
     ("Secret", "test-rbac-fernet-key"),
     ("Secret", "test-rbac-redis-password"),
-    ("Secret", "test-rbac-webserver-secret-key"),
     ("Job", "test-rbac-create-user"),
     ("Job", "test-rbac-run-airflow-migrations"),
     ("CronJob", "test-rbac-cleanup"),
@@ -121,6 +120,7 @@ def _get_object_tuples(self, version, sa: bool = True):
                     ("Service", "test-rbac-api-server"),
                     ("Deployment", "test-rbac-api-server"),
                     ("Deployment", "test-rbac-dag-processor"),
+                    ("Secret", "test-rbac-api-secret-key"),
                     ("Secret", "test-rbac-jwt-secret"),
                 )
             )
@@ -132,6 +132,7 @@ def _get_object_tuples(self, version, sa: bool = True):
                 (
                     ("Service", "test-rbac-webserver"),
                     ("Deployment", "test-rbac-webserver"),
+                    ("Secret", "test-rbac-webserver-secret-key"),
                 )
             )
             if sa:
diff --git a/helm-tests/tests/helm_tests/webserver/test_webserver.py b/helm-tests/tests/helm_tests/webserver/test_webserver.py
index d4b2a3d18873a..c70844555a2e3 100644
--- a/helm-tests/tests/helm_tests/webserver/test_webserver.py
+++ b/helm-tests/tests/helm_tests/webserver/test_webserver.py
@@ -1258,6 +1258,7 @@ class TestWebserverSecretKeySecret:
     def test_should_add_annotations_to_webserver_secret_key_secret(self):
         docs = render_chart(
             values={
+                "airflowVersion": "2.10.5",
                 "webserverSecretAnnotations": {"test_annotation": "test_annotation_value"},
             },
             show_only=["templates/secrets/webserver-secret-key-secret.yaml"],