diff --git a/install/kots/manifests/gitpod-installer-job.yaml b/install/kots/manifests/gitpod-installer-job.yaml
index 43219a6d7678db..b76de980f967f3 100644
--- a/install/kots/manifests/gitpod-installer-job.yaml
+++ b/install/kots/manifests/gitpod-installer-job.yaml
@@ -146,18 +146,36 @@ spec:
               then
                 echo "Gitpod: configuring mirrored container registry"
 
-                yq e -i ".containerRegistry.inCluster = false" "${CONFIG_FILE}"
-                yq e -i ".containerRegistry.external.url = \"{{repl LocalRegistryAddress }}\"" "${CONFIG_FILE}"
-                yq e -i ".containerRegistry.external.certificate.kind = \"secret\"" "${CONFIG_FILE}"
-                yq e -i ".containerRegistry.external.certificate.name = \"{{repl ImagePullSecretName }}\"" "${CONFIG_FILE}"
                 yq e -i ".repository = \"{{repl LocalRegistryAddress }}\"" "${CONFIG_FILE}"
                 yq e -i ".imagePullSecrets[0].kind = \"secret\"" "${CONFIG_FILE}"
                 yq e -i ".imagePullSecrets[0].name = \"{{repl ImagePullSecretName }}\"" "${CONFIG_FILE}"
                 yq e -i '.dropImageRepo = true' "${CONFIG_FILE}"
-              elif [ '{{repl ConfigOptionEquals "reg_incluster" "0" }}' = "true" ];
+              fi
+
+              # Output the local registry secret - this is proxy.replicated.com if user hasn't set their own
+              echo "{{repl LocalRegistryImagePullSecret }}" | base64 -d > /tmp/kotsregistry.json
+
+              # Add the registries to the server allowlist
+              yq e -i ".experimental.webApp.server.defaultBaseImageRegistryWhitelist += $(cat /tmp/kotsregistry.json | jq '.auths' | jq -rc 'keys')" "${CONFIG_FILE}"
+
+              if [ '{{repl ConfigOptionEquals "reg_incluster" "0" }}' = "true" ];
               then
                 echo "Gitpod: configuring external container registry"
 
+                # Create a container-registry secret merging the external registry and KOTS registry keys
+                echo '{{repl printf "{\"auths\": {\"%s\": {\"username\": \"%s\", \"password\": %s, \"auth\": \"%s\"}}}" (ConfigOption "reg_server" | default (ConfigOption "reg_url")) (ConfigOption "reg_username") (ConfigOption "reg_password" | toJson) (printf "%s:%s" (ConfigOption "reg_username") (ConfigOption "reg_password") | Base64Encode) }}' \
+                  | yq -o=json '.' - \
+                  > /tmp/gitpodregistry.json
+
+                cat /tmp/kotsregistry.json /tmp/gitpodregistry.json | jq -s '.[0] * .[1]' - - > /tmp/container-registry-secret
+
+                echo "Gitpod: create the container-registry secret"
+                kubectl create secret docker-registry container-registry \
+                  --namespace "{{repl Namespace }}" \
+                  --from-file=.dockerconfigjson=/tmp/container-registry-secret \
+                  -o yaml --dry-run=client | \
+                  kubectl replace --namespace "{{repl Namespace }}" --force -f -
+
                 yq e -i ".containerRegistry.inCluster = false" "${CONFIG_FILE}"
                 yq e -i ".containerRegistry.external.url = \"{{repl ConfigOption "reg_url" }}\"" "${CONFIG_FILE}"
                 yq e -i ".containerRegistry.external.certificate.kind = \"secret\"" "${CONFIG_FILE}"
@@ -273,6 +291,23 @@ spec:
                 'del(select(.kind == "StatefulSet" and .metadata.name == "openvsx-proxy").status)' \
                 "${GITPOD_OBJECTS}/templates/gitpod.yaml"
 
+              if [ '{{repl ConfigOptionEquals "reg_incluster" "1" }}' = "true" ];
+              then
+                echo "Gitpod: Add the local registry secret to the in-cluster registry secret"
+
+                # Get the in-cluster registry secret
+                yq eval-all '(select(.kind == "Secret" and .metadata.name == "builtin-registry-auth") | .data.".dockerconfigjson")' \
+                  "${GITPOD_OBJECTS}/templates/gitpod.yaml" \
+                  | base64 -d \
+                  > /tmp/gitpodregistry.json
+
+                export REGISTRY_SECRET=$(cat /tmp/kotsregistry.json /tmp/gitpodregistry.json | jq -s '.[0] * .[1]' - - | base64 -w 0)
+
+                echo "Gitpod: update the in-cluster registry secret"
+                yq eval-all --inplace '(select(.kind == "Secret" and .metadata.name == "builtin-registry-auth") | .data.".dockerconfigjson") |= env(REGISTRY_SECRET)' \
+                  "${GITPOD_OBJECTS}/templates/gitpod.yaml"
+              fi
+
               echo "Gitpod: Escape any Golang template values"
               sed -i -r 's/(.*\{\{.*)/{{`\1`}}/' "${GITPOD_OBJECTS}/templates/gitpod.yaml"
 
diff --git a/install/kots/manifests/gitpod-registry-secret.yaml b/install/kots/manifests/gitpod-registry-secret.yaml
deleted file mode 100644
index 121f940ce6be5a..00000000000000
--- a/install/kots/manifests/gitpod-registry-secret.yaml
+++ /dev/null
@@ -1,12 +0,0 @@
-# Copyright (c) 2022 Gitpod GmbH. All rights reserved.
-# Licensed under the MIT License. See License-MIT.txt in the project root for license information.
-
-apiVersion: v1
-kind: Secret
-metadata:
-  name: container-registry
-  annotations:
-    kots.io/when: '{{repl and (eq HasLocalRegistry false) (ConfigOptionEquals "reg_incluster" "0") }}'
-type: kubernetes.io/dockerconfigjson
-data:
-  .dockerconfigjson: '{{repl printf "{\"auths\": {\"%s\": {\"username\": \"%s\", \"password\": %s, \"auth\": \"%s\"}}}" (ConfigOption "reg_server" | default (ConfigOption "reg_url")) (ConfigOption "reg_username") (ConfigOption "reg_password" | toJson) (printf "%s:%s" (ConfigOption "reg_username") (ConfigOption "reg_password") | Base64Encode) | Base64Encode }}'
diff --git a/install/kots/manifests/kots-config.yaml b/install/kots/manifests/kots-config.yaml
index 9e0116115af863..1d69bd529d3cd9 100644
--- a/install/kots/manifests/kots-config.yaml
+++ b/install/kots/manifests/kots-config.yaml
@@ -28,7 +28,6 @@ spec:
         - name: reg_incluster
           title: Use in-cluster container registry
           type: bool
-          when: '{{repl eq HasLocalRegistry false }}'
           default: "1"
           help_text: You may either use an in-cluster container registry or configure your own external container registry for better performance. This container registry must be accessible from your Kubernetes cluster.
           recommended: false
@@ -85,27 +84,27 @@ spec:
         - name: reg_url
           title: Container registry URL
           type: text
-          when: '{{repl and (eq HasLocalRegistry false) (ConfigOptionEquals "reg_incluster" "0") }}'
+          when: '{{repl ConfigOptionEquals "reg_incluster" "0" }}'
           required: true
           help_text: The container registry URL. This will usually be the fully qualified domain of your registry.
 
         - name: reg_server
           title: Container registry server
           type: text
-          when: '{{repl and (eq HasLocalRegistry false) (ConfigOptionEquals "reg_incluster" "0") }}'
+          when: '{{repl ConfigOptionEquals "reg_incluster" "0" }}'
           help_text: The container registry server. This is used when [generating your credentials](https://kubernetes.io/docs/tasks/configure-pod-container/pull-image-private-registry/#create-a-secret-by-providing-credentials-on-the-command-line). Depending upon your provider, this may or may not be the same as the registry URL. If not specified, the URL will be used.
 
         - name: reg_username
           title: Container registry username
           type: text
-          when: '{{repl and (eq HasLocalRegistry false) (ConfigOptionEquals "reg_incluster" "0") }}'
+          when: '{{repl ConfigOptionEquals "reg_incluster" "0" }}'
           required: true
           help_text: The username for your container registry.
 
         - name: reg_password
           title: Container registry password
           type: password
-          when: '{{repl and (eq HasLocalRegistry false) (ConfigOptionEquals "reg_incluster" "0") }}'
+          when: '{{repl ConfigOptionEquals "reg_incluster" "0" }}'
           required: true
           help_text: The password for your container registry.