diff --git a/chart/templates/_helpers.yaml b/chart/templates/_helpers.yaml
index ac2798d0604b0..da417a59d4cc6 100644
--- a/chart/templates/_helpers.yaml
+++ b/chart/templates/_helpers.yaml
@@ -98,6 +98,13 @@ If release name contains chart name it will be used as a full name.
         name: {{ template "webserver_secret_key_secret" . }}
         key: webserver-secret-key
   {{- end }}
+  {{- if .Values.enableBuiltInSecretEnvVars.AIRFLOW__API_AUTH__JWT_SECRET }}
+  - name: AIRFLOW__API_AUTH__JWT_SECRET
+    valueFrom:
+      secretKeyRef:
+        name: {{ template "jwt_secret" . }}
+        key: jwt-secret
+  {{- end }}
   {{- if or (contains "CeleryExecutor" .Values.executor) (contains "CeleryKubernetesExecutor" .Values.executor) }}
     {{- if or (semverCompare "<2.4.0" .Values.airflowVersion) (.Values.data.resultBackendSecretName) (.Values.data.resultBackendConnection) }}
     {{- if .Values.enableBuiltInSecretEnvVars.AIRFLOW__CELERY__CELERY_RESULT_BACKEND }}
@@ -396,6 +403,10 @@ If release name contains chart name it will be used as a full name.
   {{- default (printf "%s-fernet-key" .Release.Name) .Values.fernetKeySecretName }}
 {{- end }}
 
+{{- define "jwt_secret" -}}
+  {{- default (printf "%s-jwt-secret" .Release.Name) .Values.jwtSecretName }}
+{{- end }}
+
 {{- define "webserver_secret_key_secret" -}}
   {{- default (printf "%s-webserver-secret-key" (include "airflow.fullname" .)) .Values.webserverSecretKeySecretName }}
 {{- end }}
diff --git a/chart/templates/secrets/jwt-secret.yaml b/chart/templates/secrets/jwt-secret.yaml
new file mode 100644
index 0000000000000..a097a55d5565c
--- /dev/null
+++ b/chart/templates/secrets/jwt-secret.yaml
@@ -0,0 +1,45 @@
+{{/*
+ 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 JWT Secret
+############################################
+{{- if not .Values.jwtSecretName }}
+{{ $generated_secret_key := (randAlphaNum 32 | b64enc) }}
+apiVersion: v1
+kind: Secret
+metadata:
+  name: {{ include "airflow.fullname" . }}-jwt-secret
+  labels:
+    tier: airflow
+    component: api-server
+    release: {{ .Release.Name }}
+    chart: {{ .Chart.Name }}
+    heritage: {{ .Release.Service }}
+    {{- with .Values.labels }}
+      {{- toYaml . | nindent 4 }}
+    {{- end }}
+  annotations:
+    "helm.sh/hook": "pre-install"
+    "helm.sh/hook-delete-policy": "before-hook-creation"
+    "helm.sh/hook-weight": "0"
+type: Opaque
+data:
+  jwt-secret: {{ (default $generated_secret_key .Values.jwtSecret) | b64enc | quote }}
+{{- end }}
diff --git a/chart/values.schema.json b/chart/values.schema.json
index 614399d4d51e3..79583aada47fd 100644
--- a/chart/values.schema.json
+++ b/chart/values.schema.json
@@ -1064,6 +1064,11 @@
                     "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",
+                    "default": true
+                },
                 "AIRFLOW__WEBSERVER__SECRET_KEY": {
                     "description": "Enable ``AIRFLOW__WEBSERVER__SECRET_KEY`` variable to be read from the Webserver Secret Key Secret",
                     "type": "boolean",
@@ -1459,6 +1464,24 @@
                 "type": "string"
             }
         },
+        "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": [
+                "string",
+                "null"
+            ],
+            "x-docsSection": "Common",
+            "default": null
+        },
+        "jwtSecretName": {
+            "description": "The JWT secret name.",
+            "type": [
+                "string",
+                "null"
+            ],
+            "x-docsSection": "Airflow",
+            "default": null
+        },
         "webserverSecretKey": {
             "description": "The Flask secret key for Airflow Webserver to encrypt browser session.",
             "type": [
diff --git a/chart/values.yaml b/chart/values.yaml
index 524af23122779..4fed9574bd21d 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_AUTH__JWT_SECRET: true
   AIRFLOW__WEBSERVER__SECRET_KEY: true
   AIRFLOW__CELERY__CELERY_RESULT_BACKEND: true
   AIRFLOW__CELERY__RESULT_BACKEND: true
@@ -556,6 +557,10 @@ webserverSecretKey: ~
 webserverSecretAnnotations: {}
 webserverSecretKeySecretName: ~
 
+# Secret key used to encode and decode JWTs: `[api_auth] jwt_secret` in airflow.cfg
+jwtSecret: ~
+jwtSecretName: ~
+
 # 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 78b43d02f73eb..e6b247afb1cd0 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_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
                     "AIRFLOW__ELASTICSEARCH__HOST": False,
@@ -370,6 +371,7 @@ def test_have_all_variables(self):
             "AIRFLOW__DATABASE__SQL_ALCHEMY_CONN",
             "AIRFLOW_CONN_AIRFLOW_DB",
             "AIRFLOW__WEBSERVER__SECRET_KEY",
+            "AIRFLOW__API_AUTH__JWT_SECRET",
             "AIRFLOW__CELERY__BROKER_URL",
         ]
         expected_vars_in_worker = ["DUMB_INIT_SETSID"] + expected_vars
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 91829848f8ea2..d7977f7e5281e 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
@@ -38,6 +38,7 @@
     ("Secret", "test-basic-airflow-metadata"),
     ("Secret", "test-basic-broker-url"),
     ("Secret", "test-basic-fernet-key"),
+    ("Secret", "test-basic-airflow-jwt-secret"),
     ("Secret", "test-basic-airflow-webserver-secret-key"),
     ("Secret", "test-basic-redis-password"),
     ("Secret", "test-basic-postgresql"),
@@ -136,6 +137,7 @@ def test_basic_deployments(self, version):
             ("Secret", "test-basic-metadata"),
             ("Secret", "test-basic-broker-url"),
             ("Secret", "test-basic-fernet-key"),
+            ("Secret", "test-basic-jwt-secret"),
             ("Secret", "test-basic-webserver-secret-key"),
             ("Secret", "test-basic-postgresql"),
             ("Secret", "test-basic-redis-password"),
@@ -236,6 +238,7 @@ 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-jwt-secret"),
             ("Secret", "test-basic-webserver-secret-key"),
             ("Secret", "test-basic-postgresql"),
             ("Secret", "test-basic-redis-password"),
diff --git a/helm-tests/tests/helm_tests/security/test_rbac.py b/helm-tests/tests/helm_tests/security/test_rbac.py
index 6271e7cfafcf0..fcd578daa608e 100644
--- a/helm-tests/tests/helm_tests/security/test_rbac.py
+++ b/helm-tests/tests/helm_tests/security/test_rbac.py
@@ -46,6 +46,7 @@
     ("StatefulSet", "test-rbac-worker"),
     ("Secret", "test-rbac-broker-url"),
     ("Secret", "test-rbac-fernet-key"),
+    ("Secret", "test-rbac-jwt-secret"),
     ("Secret", "test-rbac-redis-password"),
     ("Secret", "test-rbac-webserver-secret-key"),
     ("Job", "test-rbac-create-user"),