diff --git a/dev/breeze/doc/images/output_start-airflow.svg b/dev/breeze/doc/images/output_start-airflow.svg
index 8727370a3e565..3c2e4ef5a37fd 100644
--- a/dev/breeze/doc/images/output_start-airflow.svg
+++ b/dev/breeze/doc/images/output_start-airflow.svg
@@ -1,4 +1,4 @@
-<svg class="rich-terminal" viewBox="0 0 1482 3710.0" xmlns="http://www.w3.org/2000/svg">
+<svg class="rich-terminal" viewBox="0 0 1482 3807.6" xmlns="http://www.w3.org/2000/svg">
     <!-- Generated with Rich https://www.textualize.io -->
     <style>
 
@@ -43,7 +43,7 @@
 
     <defs>
     <clipPath id="breeze-start-airflow-clip-terminal">
-      <rect x="0" y="0" width="1463.0" height="3659.0" />
+      <rect x="0" y="0" width="1463.0" height="3756.6" />
     </clipPath>
     <clipPath id="breeze-start-airflow-line-0">
     <rect x="0" y="1.5" width="1464" height="24.65"/>
@@ -492,9 +492,21 @@
 <clipPath id="breeze-start-airflow-line-148">
     <rect x="0" y="3612.7" width="1464" height="24.65"/>
             </clipPath>
+<clipPath id="breeze-start-airflow-line-149">
+    <rect x="0" y="3637.1" width="1464" height="24.65"/>
+            </clipPath>
+<clipPath id="breeze-start-airflow-line-150">
+    <rect x="0" y="3661.5" width="1464" height="24.65"/>
+            </clipPath>
+<clipPath id="breeze-start-airflow-line-151">
+    <rect x="0" y="3685.9" width="1464" height="24.65"/>
+            </clipPath>
+<clipPath id="breeze-start-airflow-line-152">
+    <rect x="0" y="3710.3" width="1464" height="24.65"/>
+            </clipPath>
     </defs>
 
-    <rect fill="#292929" stroke="rgba(255,255,255,0.35)" stroke-width="1" x="1" y="1" width="1480" height="3708" rx="8"/><text class="breeze-start-airflow-title" fill="#c5c8c6" text-anchor="middle" x="740" y="27">Command:&#160;start-airflow</text>
+    <rect fill="#292929" stroke="rgba(255,255,255,0.35)" stroke-width="1" x="1" y="1" width="1480" height="3805.6" rx="8"/><text class="breeze-start-airflow-title" fill="#c5c8c6" text-anchor="middle" x="740" y="27">Command:&#160;start-airflow</text>
             <g transform="translate(26,22)">
             <circle cx="0" cy="0" r="7" fill="#ff5f57"/>
             <circle cx="22" cy="0" r="7" fill="#febc2e"/>
@@ -648,12 +660,16 @@
 </text><text class="breeze-start-airflow-r5" x="0" y="3460.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-141)">│</text><text class="breeze-start-airflow-r7" x="195.2" y="3460.4" textLength="1244.4" clip-path="url(#breeze-start-airflow-line-141)">(scheduler&#160;|&#160;triggerer&#160;|&#160;api-server&#160;|&#160;dag-processor&#160;|&#160;edge-worker&#160;|&#160;celery-worker)&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;</text><text class="breeze-start-airflow-r5" x="1451.8" y="3460.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-141)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3460.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-141)">
 </text><text class="breeze-start-airflow-r5" x="0" y="3484.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-142)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3484.8" textLength="122" clip-path="url(#breeze-start-airflow-line-142)">--debugger</text><text class="breeze-start-airflow-r1" x="195.2" y="3484.8" textLength="597.8" clip-path="url(#breeze-start-airflow-line-142)">Debugger&#160;to&#160;use&#160;for&#160;debugging&#160;Airflow&#160;components.</text><text class="breeze-start-airflow-r7" x="805.2" y="3484.8" textLength="317.2" clip-path="url(#breeze-start-airflow-line-142)">(debugpy&#160;|&#160;pydevd-pycharm)</text><text class="breeze-start-airflow-r5" x="1134.6" y="3484.8" textLength="219.6" clip-path="url(#breeze-start-airflow-line-142)">[default:&#160;debugpy]</text><text class="breeze-start-airflow-r5" x="1451.8" y="3484.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-142)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3484.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-142)">
 </text><text class="breeze-start-airflow-r5" x="0" y="3509.2" textLength="1464" clip-path="url(#breeze-start-airflow-line-143)">╰──────────────────────────────────────────────────────────────────────────────────────────────────────────────────────╯</text><text class="breeze-start-airflow-r1" x="1464" y="3509.2" textLength="12.2" clip-path="url(#breeze-start-airflow-line-143)">
-</text><text class="breeze-start-airflow-r5" x="0" y="3533.6" textLength="24.4" clip-path="url(#breeze-start-airflow-line-144)">╭─</text><text class="breeze-start-airflow-r5" x="24.4" y="3533.6" textLength="195.2" clip-path="url(#breeze-start-airflow-line-144)">&#160;Common&#160;options&#160;</text><text class="breeze-start-airflow-r5" x="219.6" y="3533.6" textLength="1220" clip-path="url(#breeze-start-airflow-line-144)">────────────────────────────────────────────────────────────────────────────────────────────────────</text><text class="breeze-start-airflow-r5" x="1439.6" y="3533.6" textLength="24.4" clip-path="url(#breeze-start-airflow-line-144)">─╮</text><text class="breeze-start-airflow-r1" x="1464" y="3533.6" textLength="12.2" clip-path="url(#breeze-start-airflow-line-144)">
-</text><text class="breeze-start-airflow-r5" x="0" y="3558" textLength="12.2" clip-path="url(#breeze-start-airflow-line-145)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3558" textLength="97.6" clip-path="url(#breeze-start-airflow-line-145)">--answer</text><text class="breeze-start-airflow-r6" x="158.6" y="3558" textLength="24.4" clip-path="url(#breeze-start-airflow-line-145)">-a</text><text class="breeze-start-airflow-r1" x="207.4" y="3558" textLength="317.2" clip-path="url(#breeze-start-airflow-line-145)">Force&#160;answer&#160;to&#160;questions.</text><text class="breeze-start-airflow-r7" x="536.8" y="3558" textLength="353.8" clip-path="url(#breeze-start-airflow-line-145)">(y&#160;|&#160;n&#160;|&#160;q&#160;|&#160;yes&#160;|&#160;no&#160;|&#160;quit)</text><text class="breeze-start-airflow-r5" x="1451.8" y="3558" textLength="12.2" clip-path="url(#breeze-start-airflow-line-145)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3558" textLength="12.2" clip-path="url(#breeze-start-airflow-line-145)">
-</text><text class="breeze-start-airflow-r5" x="0" y="3582.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-146)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3582.4" textLength="109.8" clip-path="url(#breeze-start-airflow-line-146)">--dry-run</text><text class="breeze-start-airflow-r6" x="158.6" y="3582.4" textLength="24.4" clip-path="url(#breeze-start-airflow-line-146)">-D</text><text class="breeze-start-airflow-r1" x="207.4" y="3582.4" textLength="719.8" clip-path="url(#breeze-start-airflow-line-146)">If&#160;dry-run&#160;is&#160;set,&#160;commands&#160;are&#160;only&#160;printed,&#160;not&#160;executed.</text><text class="breeze-start-airflow-r5" x="1451.8" y="3582.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-146)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3582.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-146)">
-</text><text class="breeze-start-airflow-r5" x="0" y="3606.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-147)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3606.8" textLength="109.8" clip-path="url(#breeze-start-airflow-line-147)">--verbose</text><text class="breeze-start-airflow-r6" x="158.6" y="3606.8" textLength="24.4" clip-path="url(#breeze-start-airflow-line-147)">-v</text><text class="breeze-start-airflow-r1" x="207.4" y="3606.8" textLength="585.6" clip-path="url(#breeze-start-airflow-line-147)">Print&#160;verbose&#160;information&#160;about&#160;performed&#160;steps.</text><text class="breeze-start-airflow-r5" x="1451.8" y="3606.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-147)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3606.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-147)">
-</text><text class="breeze-start-airflow-r5" x="0" y="3631.2" textLength="12.2" clip-path="url(#breeze-start-airflow-line-148)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3631.2" textLength="73.2" clip-path="url(#breeze-start-airflow-line-148)">--help</text><text class="breeze-start-airflow-r6" x="158.6" y="3631.2" textLength="24.4" clip-path="url(#breeze-start-airflow-line-148)">-h</text><text class="breeze-start-airflow-r1" x="207.4" y="3631.2" textLength="329.4" clip-path="url(#breeze-start-airflow-line-148)">Show&#160;this&#160;message&#160;and&#160;exit.</text><text class="breeze-start-airflow-r5" x="1451.8" y="3631.2" textLength="12.2" clip-path="url(#breeze-start-airflow-line-148)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3631.2" textLength="12.2" clip-path="url(#breeze-start-airflow-line-148)">
-</text><text class="breeze-start-airflow-r5" x="0" y="3655.6" textLength="1464" clip-path="url(#breeze-start-airflow-line-149)">╰──────────────────────────────────────────────────────────────────────────────────────────────────────────────────────╯</text><text class="breeze-start-airflow-r1" x="1464" y="3655.6" textLength="12.2" clip-path="url(#breeze-start-airflow-line-149)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3533.6" textLength="24.4" clip-path="url(#breeze-start-airflow-line-144)">╭─</text><text class="breeze-start-airflow-r5" x="24.4" y="3533.6" textLength="97.6" clip-path="url(#breeze-start-airflow-line-144)">&#160;config&#160;</text><text class="breeze-start-airflow-r5" x="122" y="3533.6" textLength="1317.6" clip-path="url(#breeze-start-airflow-line-144)">────────────────────────────────────────────────────────────────────────────────────────────────────────────</text><text class="breeze-start-airflow-r5" x="1439.6" y="3533.6" textLength="24.4" clip-path="url(#breeze-start-airflow-line-144)">─╮</text><text class="breeze-start-airflow-r1" x="1464" y="3533.6" textLength="12.2" clip-path="url(#breeze-start-airflow-line-144)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3558" textLength="12.2" clip-path="url(#breeze-start-airflow-line-145)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3558" textLength="256.2" clip-path="url(#breeze-start-airflow-line-145)">--template-searchpath</text><text class="breeze-start-airflow-r1" x="329.4" y="3558" textLength="671" clip-path="url(#breeze-start-airflow-line-145)">Specify&#160;the&#160;template&#160;search&#160;path&#160;to&#160;use&#160;inside&#160;Airflow.</text><text class="breeze-start-airflow-r7" x="1012.6" y="3558" textLength="73.2" clip-path="url(#breeze-start-airflow-line-145)">(TEXT)</text><text class="breeze-start-airflow-r5" x="1451.8" y="3558" textLength="12.2" clip-path="url(#breeze-start-airflow-line-145)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3558" textLength="12.2" clip-path="url(#breeze-start-airflow-line-145)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3582.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-146)">│</text><text class="breeze-start-airflow-r5" x="329.4" y="3582.4" textLength="671" clip-path="url(#breeze-start-airflow-line-146)">[default:&#160;/opt/airflow/dags/include]&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;</text><text class="breeze-start-airflow-r5" x="1451.8" y="3582.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-146)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3582.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-146)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3606.8" textLength="1464" clip-path="url(#breeze-start-airflow-line-147)">╰──────────────────────────────────────────────────────────────────────────────────────────────────────────────────────╯</text><text class="breeze-start-airflow-r1" x="1464" y="3606.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-147)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3631.2" textLength="24.4" clip-path="url(#breeze-start-airflow-line-148)">╭─</text><text class="breeze-start-airflow-r5" x="24.4" y="3631.2" textLength="195.2" clip-path="url(#breeze-start-airflow-line-148)">&#160;Common&#160;options&#160;</text><text class="breeze-start-airflow-r5" x="219.6" y="3631.2" textLength="1220" clip-path="url(#breeze-start-airflow-line-148)">────────────────────────────────────────────────────────────────────────────────────────────────────</text><text class="breeze-start-airflow-r5" x="1439.6" y="3631.2" textLength="24.4" clip-path="url(#breeze-start-airflow-line-148)">─╮</text><text class="breeze-start-airflow-r1" x="1464" y="3631.2" textLength="12.2" clip-path="url(#breeze-start-airflow-line-148)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3655.6" textLength="12.2" clip-path="url(#breeze-start-airflow-line-149)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3655.6" textLength="97.6" clip-path="url(#breeze-start-airflow-line-149)">--answer</text><text class="breeze-start-airflow-r6" x="158.6" y="3655.6" textLength="24.4" clip-path="url(#breeze-start-airflow-line-149)">-a</text><text class="breeze-start-airflow-r1" x="207.4" y="3655.6" textLength="317.2" clip-path="url(#breeze-start-airflow-line-149)">Force&#160;answer&#160;to&#160;questions.</text><text class="breeze-start-airflow-r7" x="536.8" y="3655.6" textLength="353.8" clip-path="url(#breeze-start-airflow-line-149)">(y&#160;|&#160;n&#160;|&#160;q&#160;|&#160;yes&#160;|&#160;no&#160;|&#160;quit)</text><text class="breeze-start-airflow-r5" x="1451.8" y="3655.6" textLength="12.2" clip-path="url(#breeze-start-airflow-line-149)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3655.6" textLength="12.2" clip-path="url(#breeze-start-airflow-line-149)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3680" textLength="12.2" clip-path="url(#breeze-start-airflow-line-150)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3680" textLength="109.8" clip-path="url(#breeze-start-airflow-line-150)">--dry-run</text><text class="breeze-start-airflow-r6" x="158.6" y="3680" textLength="24.4" clip-path="url(#breeze-start-airflow-line-150)">-D</text><text class="breeze-start-airflow-r1" x="207.4" y="3680" textLength="719.8" clip-path="url(#breeze-start-airflow-line-150)">If&#160;dry-run&#160;is&#160;set,&#160;commands&#160;are&#160;only&#160;printed,&#160;not&#160;executed.</text><text class="breeze-start-airflow-r5" x="1451.8" y="3680" textLength="12.2" clip-path="url(#breeze-start-airflow-line-150)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3680" textLength="12.2" clip-path="url(#breeze-start-airflow-line-150)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3704.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-151)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3704.4" textLength="109.8" clip-path="url(#breeze-start-airflow-line-151)">--verbose</text><text class="breeze-start-airflow-r6" x="158.6" y="3704.4" textLength="24.4" clip-path="url(#breeze-start-airflow-line-151)">-v</text><text class="breeze-start-airflow-r1" x="207.4" y="3704.4" textLength="585.6" clip-path="url(#breeze-start-airflow-line-151)">Print&#160;verbose&#160;information&#160;about&#160;performed&#160;steps.</text><text class="breeze-start-airflow-r5" x="1451.8" y="3704.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-151)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3704.4" textLength="12.2" clip-path="url(#breeze-start-airflow-line-151)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3728.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-152)">│</text><text class="breeze-start-airflow-r4" x="24.4" y="3728.8" textLength="73.2" clip-path="url(#breeze-start-airflow-line-152)">--help</text><text class="breeze-start-airflow-r6" x="158.6" y="3728.8" textLength="24.4" clip-path="url(#breeze-start-airflow-line-152)">-h</text><text class="breeze-start-airflow-r1" x="207.4" y="3728.8" textLength="329.4" clip-path="url(#breeze-start-airflow-line-152)">Show&#160;this&#160;message&#160;and&#160;exit.</text><text class="breeze-start-airflow-r5" x="1451.8" y="3728.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-152)">│</text><text class="breeze-start-airflow-r1" x="1464" y="3728.8" textLength="12.2" clip-path="url(#breeze-start-airflow-line-152)">
+</text><text class="breeze-start-airflow-r5" x="0" y="3753.2" textLength="1464" clip-path="url(#breeze-start-airflow-line-153)">╰──────────────────────────────────────────────────────────────────────────────────────────────────────────────────────╯</text><text class="breeze-start-airflow-r1" x="1464" y="3753.2" textLength="12.2" clip-path="url(#breeze-start-airflow-line-153)">
 </text>
     </g>
     </g>
diff --git a/dev/breeze/doc/images/output_start-airflow.txt b/dev/breeze/doc/images/output_start-airflow.txt
index 71762a7917f05..6d91ce31668bb 100644
--- a/dev/breeze/doc/images/output_start-airflow.txt
+++ b/dev/breeze/doc/images/output_start-airflow.txt
@@ -1 +1 @@
-6d48fc396beb2ab18c5e85071656a293
+bafda7edfe9d6ac17297d32f90fa87a3
diff --git a/dev/breeze/src/airflow_breeze/commands/developer_commands.py b/dev/breeze/src/airflow_breeze/commands/developer_commands.py
index 7d39ffa4b83fc..5658ac64c1680 100644
--- a/dev/breeze/src/airflow_breeze/commands/developer_commands.py
+++ b/dev/breeze/src/airflow_breeze/commands/developer_commands.py
@@ -96,6 +96,7 @@
     DEFAULT_ALLOWED_EXECUTOR,
     DEFAULT_CELERY_BROKER,
     DEFAULT_PYTHON_MAJOR_MINOR_VERSION,
+    DEFAULT_TEMPLATE_SEARCHPATH,
     GITHUB_REPO_BRANCH_PATTERN,
     MOUNT_ALL,
     START_AIRFLOW_ALLOWED_EXECUTORS,
@@ -498,6 +499,15 @@ def shell(
     show_default=True,
 )
 
+option_template_searchpath = click.option(
+    "--template-searchpath",
+    type=str,
+    help="Specify the template search path to use inside Airflow.",
+    default=DEFAULT_TEMPLATE_SEARCHPATH,
+    envvar="AIRFLOW__CORE__TEMPLATE_SEARCHPATH",
+    show_default=True,
+)
+
 
 @main.command(name="start-airflow")
 @click.option(
@@ -557,6 +567,7 @@ def shell(
 @option_allow_pre_releases
 @option_use_distributions_from_dist
 @option_verbose
+@option_template_searchpath
 def start_airflow(
     airflow_constraints_mode: str,
     airflow_constraints_location: str,
@@ -602,6 +613,7 @@ def start_airflow(
     use_distributions_from_dist: bool,
     use_uv: bool,
     uv_http_timeout: int,
+    template_searchpath: str,
 ):
     """
     Enter breeze environment and starts all Airflow components in the tmux session.
@@ -675,6 +687,7 @@ def start_airflow(
         use_distributions_from_dist=use_distributions_from_dist,
         use_uv=use_uv,
         uv_http_timeout=uv_http_timeout,
+        template_searchpath=template_searchpath,
     )
     rebuild_or_pull_ci_image_if_needed(command_params=shell_params)
     result = enter_shell(shell_params=shell_params)
diff --git a/dev/breeze/src/airflow_breeze/commands/developer_commands_config.py b/dev/breeze/src/airflow_breeze/commands/developer_commands_config.py
index b4332f7c1a665..09de279070e21 100644
--- a/dev/breeze/src/airflow_breeze/commands/developer_commands_config.py
+++ b/dev/breeze/src/airflow_breeze/commands/developer_commands_config.py
@@ -297,6 +297,7 @@
             "name": "Debugging options",
             "options": ["--debug", "--debugger"],
         },
+        {"name": "config", "options": ["--template-searchpath"]},
     ],
     "breeze exec": [
         {"name": "Drops in the interactive shell of active airflow container"},
diff --git a/dev/breeze/src/airflow_breeze/global_constants.py b/dev/breeze/src/airflow_breeze/global_constants.py
index 4fcb9c261a7cc..3864c8998e7f7 100644
--- a/dev/breeze/src/airflow_breeze/global_constants.py
+++ b/dev/breeze/src/airflow_breeze/global_constants.py
@@ -794,3 +794,7 @@ class GithubEvents(Enum):
 @clearable_cache
 def github_events() -> list[str]:
     return [e.value for e in GithubEvents]
+
+
+# Define the default template path
+DEFAULT_TEMPLATE_SEARCHPATH = "/opt/airflow/dags/include"
diff --git a/dev/breeze/src/airflow_breeze/params/shell_params.py b/dev/breeze/src/airflow_breeze/params/shell_params.py
index 660893a9e6e80..63573f356cc71 100644
--- a/dev/breeze/src/airflow_breeze/params/shell_params.py
+++ b/dev/breeze/src/airflow_breeze/params/shell_params.py
@@ -47,6 +47,7 @@
     CELERY_BROKER_URLS_MAP,
     CELERY_EXECUTOR,
     DEFAULT_CELERY_BROKER,
+    DEFAULT_TEMPLATE_SEARCHPATH,
     DEFAULT_UV_HTTP_TIMEOUT,
     DOCKER_DEFAULT_PLATFORM,
     DRILL_HOST_PORT,
@@ -230,6 +231,7 @@ class ShellParams:
     verbose_commands: bool = False
     version_suffix: str = ""
     warn_image_upgrade_needed: bool = False
+    template_searchpath: str = DEFAULT_TEMPLATE_SEARCHPATH
 
     def clone_with_test(self, test_type: str) -> ShellParams:
         new_params = deepcopy(self)
@@ -542,6 +544,7 @@ def env_variables_for_docker_commands(self) -> dict[str, str]:
         _set_var(_env, "AIRFLOW__CELERY__BROKER_URL", self.airflow_celery_broker_url)
         _set_var(_env, "AIRFLOW__CORE__AUTH_MANAGER", self.auth_manager_path)
         _set_var(_env, "AIRFLOW__CORE__EXECUTOR", self.executor)
+        _set_var(_env, "AIRFLOW__CORE__TEMPLATE_SEARCHPATH", self.template_searchpath)
         if self.auth_manager == SIMPLE_AUTH_MANAGER:
             _set_var(_env, "AIRFLOW__CORE__SIMPLE_AUTH_MANAGER_USERS", "admin:admin,viewer:viewer")
         _set_var(