diff --git a/.github/ISSUE_TEMPLATE/kubernetes_bump.md b/.github/ISSUE_TEMPLATE/kubernetes_bump.md
index 9b65aec8d365..a6ea6b646253 100644
--- a/.github/ISSUE_TEMPLATE/kubernetes_bump.md
+++ b/.github/ISSUE_TEMPLATE/kubernetes_bump.md
@@ -34,21 +34,25 @@ changes should be cherry-picked to all release series that will support the new
     * Note: Only bump for Cluster API versions that will support the new Kubernetes release.
   * Prior art: #9160
 * [ ] Ensure the jobs are adjusted to provide test coverage according to our [support policy](https://cluster-api.sigs.k8s.io/reference/versions.html#supported-kubernetes-versions):
-  * For the main branch:
-    * periodics:
-      * Drop the oldest upgrade job as the oldest Kubernetes minor version is now out of support.
-      * Add new upgrade job which upgrades from the previous to the new Kubernetes version.
-    * periodics & presubmits:
-      * Bump `KUBERNETES_VERSION_MANAGEMENT` of the `e2e-mink8s` job to the new minimum supported management cluster version.
-      * Bump `KUBEBUILDER_ENVTEST_KUBERNETES_VERSION` of the `test-mink8s` jobs to the new minimum supported management cluster version.
-      * Adjust the `-latest` upgrade job to upgrade from the new Kubernetes to the next Kubernetes version.
-  * For the release branch of the latest supported Cluster API minor release:
-    * periodics & presubmits:
-      * Adust the `-latest` upgrade jobs to upgrade to the new Kubernetes version instead of latest.
-  * Note: Also check if `ETCD_VERSION_UPGRADE_TO` or `COREDNS_VERSION_UPGRADE_TO` needs to change for the upgrades jobs to the new or next Kubernetes version.
-    * For etcd, see the `DefaultEtcdVersion` kubeadm constant: [e.g. for v1.28.0](https://github.com/kubernetes/kubernetes/blob/v1.28.0/cmd/kubeadm/app/constants/constants.go#L308)
-    * For coredns, see the `CoreDNSVersion` kubeadm constant:[e.g. for v1.28.0](https://github.com/kubernetes/kubernetes/blob/v1.28.0/cmd/kubeadm/app/constants/constants.go#L344)
-  * Prior art: https://github.com/kubernetes/test-infra/pull/30347 https://github.com/kubernetes/test-infra/pull/30406 https://github.com/kubernetes/test-infra/pull/30407
+
+  * At the `.versions`  section in the `cluster-api-prowjob-gen.yaml` file in [test-infra](https://github.com/kubernetes/test-infra/blob/master/config/jobs/kubernetes-sigs/cluster-api/):
+    * Add a new entry for the new Kubernetes version
+    * Adjust the released kKubernetes's version entry to refer `stable-1.<minor>` instead of `ci/latest-1.<minor>`
+    * Check and update the versions for the keys `etcd` and `coreDNS` if necessary:
+      * For etcd, see the `DefaultEtcdVersion` kubeadm constant: [e.g. for v1.28.0](https://github.com/kubernetes/kubernetes/blob/v1.28.0/cmd/kubeadm/app/constants/constants.go#L308)
+      * For coredns, see the `CoreDNSVersion` kubeadm constant:[e.g. for v1.28.0](https://github.com/kubernetes/kubernetes/blob/v1.28.0/cmd/kubeadm/app/constants/constants.go#L344)
+  * For the `.branches.main` section in the `cluster-api-prowjob-gen.yaml` file in [test-infra](https://github.com/kubernetes/test-infra/blob/master/config/jobs/kubernetes-sigs/cluster-api/):
+    * For the `.upgrades` section:
+      * Drop the oldest upgrade
+      * Add a new upgrade entry from the previous to the new Kubernetes version
+    * Bump the version set at `.kubernetesVersionManagement` to the new minimum supported management cluster version (This is the image version available as kind image).
+    * Bump the version set at `.kubebuilderEnvtestKubernetesVersion` to the new minimum supported management cluster version.
+  * Run `make generate-test-infra-prowjobs` to generate the resulting prowjob configuration:
+
+    ```sh
+    TEST_INFRA_DIR=../../k8s.io/test-infra make generate-test-infra-prowjobs
+    ```
+
 * [ ] Update book:
   * Update supported versions in `versions.md`
   * Update job documentation in `jobs.md`
@@ -65,7 +69,7 @@ need them in older releases as they are not necessary to manage workload cluster
 run the Cluster API controllers on the new Kubernetes version.
 
 * [ ] Ensure there is a new controller-runtime minor release which uses the new Kubernetes Go dependencies.
-* [ ] Update our Prow jobs for the `main` branch to use the correct `kubekins-e2e` image
+* [ ] Update our Prow jobs for the `main` branch to use the correct `kubekins-e2e` image via the configuration file and by running `make generate-test-infra-prowjobs`.
   * It is recommended to have one PR for presubmit and one for periodic jobs to reduce the risk of breaking the periodic jobs.
   * Prior art: presubmit jobs: https://github.com/kubernetes/test-infra/pull/27311
   * Prior art: periodic jobs: https://github.com/kubernetes/test-infra/pull/27326
diff --git a/Makefile b/Makefile
index cb0425f3e350..e830ea893d69 100644
--- a/Makefile
+++ b/Makefile
@@ -190,6 +190,9 @@ OPENAPI_GEN_BIN := openapi-gen
 OPENAPI_GEN := $(abspath $(TOOLS_BIN_DIR)/$(OPENAPI_GEN_BIN))
 OPENAPI_GEN_PKG := k8s.io/kube-openapi/cmd/openapi-gen
 
+PROWJOB_GEN_BIN := prowjob-gen
+PROWJOB_GEN := $(abspath $(TOOLS_BIN_DIR)/$(PROWJOB_GEN_BIN))
+
 RUNTIME_OPENAPI_GEN_BIN := runtime-openapi-gen
 RUNTIME_OPENAPI_GEN := $(abspath $(TOOLS_BIN_DIR)/$(RUNTIME_OPENAPI_GEN_BIN))
 
@@ -600,6 +603,13 @@ generate-diagrams-book: ## Generate diagrams for *.plantuml files in book
 generate-diagrams-proposals: ## Generate diagrams for *.plantuml files in proposals
 	docker run -v $(ROOT_DIR)/$(DOCS_DIR):/$(DOCS_DIR)$(DOCKER_VOL_OPTS)  plantuml/plantuml:$(PLANTUML_VER) /$(DOCS_DIR)/proposals/**/*.plantuml
 
+.PHONY: generate-test-infra-prowjobs
+generate-test-infra-prowjobs: $(PROWJOB_GEN) ## Generates the prowjob configurations in test-infra
+	@if [ -z "${TEST_INFRA_DIR}" ]; then echo "TEST_INFRA_DIR is not set"; exit 1; fi
+	$(PROWJOB_GEN) \
+		-config "$(TEST_INFRA_DIR)/config/jobs/kubernetes-sigs/cluster-api/cluster-api-prowjob-gen.yaml" \
+		-templates-dir "$(TEST_INFRA_DIR)/config/jobs/kubernetes-sigs/cluster-api/templates" \
+		-output-dir "$(TEST_INFRA_DIR)/config/jobs/kubernetes-sigs/cluster-api"
 
 ## --------------------------------------
 ## Lint / Verify
@@ -1307,6 +1317,9 @@ $(OPENAPI_GEN_BIN): $(OPENAPI_GEN) ## Build a local copy of openapi-gen.
 .PHONY: $(RUNTIME_OPENAPI_GEN_BIN)
 $(RUNTIME_OPENAPI_GEN_BIN): $(RUNTIME_OPENAPI_GEN) ## Build a local copy of runtime-openapi-gen.
 
+.PHONY: $(PROWJOB_GEN_BIN)
+$(PROWJOB_GEN_BIN): $(PROWJOB_GEN) ## Build a local copy of prowjob-gen.
+
 .PHONY: $(CONVERSION_VERIFIER_BIN)
 $(CONVERSION_VERIFIER_BIN): $(CONVERSION_VERIFIER) ## Build a local copy of conversion-verifier.
 
@@ -1367,6 +1380,10 @@ $(OPENAPI_GEN): # Build openapi-gen from tools folder.
 $(RUNTIME_OPENAPI_GEN): $(TOOLS_DIR)/go.mod # Build openapi-gen from tools folder.
 	cd $(TOOLS_DIR); go build -tags=tools -o $(BIN_DIR)/$(RUNTIME_OPENAPI_GEN_BIN) sigs.k8s.io/cluster-api/hack/tools/runtime-openapi-gen
 
+.PHONY: $(PROWJOB_GEN)
+$(PROWJOB_GEN): $(TOOLS_DIR)/go.mod # Build prowjob-gen from tools folder.
+	cd $(TOOLS_DIR); go build -tags=tools -o $(BIN_DIR)/$(PROWJOB_GEN_BIN) sigs.k8s.io/cluster-api/hack/tools/prowjob-gen
+
 $(GOTESTSUM): # Build gotestsum from tools folder.
 	GOBIN=$(TOOLS_BIN_DIR) $(GO_INSTALL) $(GOTESTSUM_PKG) $(GOTESTSUM_BIN) $(GOTESTSUM_VER)
 
diff --git a/hack/boilerplate/boilerplate.py b/hack/boilerplate/boilerplate.py
index 830fcdd3e842..7a9fb6155645 100755
--- a/hack/boilerplate/boilerplate.py
+++ b/hack/boilerplate/boilerplate.py
@@ -143,6 +143,7 @@ def file_passes(filename, refs, regexs):
             for line in difflib.unified_diff(ref, data, 'reference', filename, lineterm=''):
                 print(line, file=verbose_out)
             print(file=verbose_out)
+
         return False
 
     return True
@@ -154,7 +155,10 @@ def file_extension(filename):
 
 # list all the files contain 'DO NOT EDIT', but are not generated
 skipped_ungenerated_files = [
-    'hack/lib/swagger.sh', 'hack/boilerplate/boilerplate.py']
+    'hack/lib/swagger.sh',
+    'hack/boilerplate/boilerplate.py',
+    '/hack/tools/prowjob-gen/generator.go',
+    ]
 
 def normalize_files(files):
     newfiles = []
diff --git a/hack/tools/prowjob-gen/README.md b/hack/tools/prowjob-gen/README.md
new file mode 100644
index 000000000000..5333aa130616
--- /dev/null
+++ b/hack/tools/prowjob-gen/README.md
@@ -0,0 +1,68 @@
+# prowjob-gen
+
+Prowjob-gen is a tool which helps generating prowjob configuration.
+
+## Usage
+
+Flags:
+
+```txt
+  -config string
+        Path to the config file
+  -output-dir string
+        Path to the directory to create the files in
+  -templates-dir string
+        Path to the directory containing the template files referenced inside the config file
+```
+
+When running prowjob-gen, all flags need to be provided.
+The tool then will iterate over all templates defined in the config file and execute them per configured branch.
+
+The configuration file is supposed to be in yaml format and to be stored inside the [test-infra](https://github.com/kubernetes/test-infra)
+repository, we have to make sure it is not getting parsed as configuration for prow.
+Because of that the top-level key for the configuration file is `prow-ignored:`.
+
+A sample configuration looks as follows:
+
+```yaml
+prow_ignored:
+  branches:
+    main: # values below the branch here are available in the template 
+      kubekinsImage: "gcr.io/k8s-staging-test-infra/kubekins-e2e:v20231208-8b9fd88e88-1.29"
+      interval: "2h"
+      kubernetesVersionManagement: "v1.26.6@sha256:6e2d8b28a5b601defe327b98bd1c2d1930b49e5d8c512e1895099e4504007adb"
+      kubebuilderEnvtestKubernetesVersion: "1.26.1"
+      upgrades:
+      - from: "1.29"
+        to: "1.30"
+
+  templates:
+  - name: "cluster-api-periodics.yaml.tpl"
+    format: "cluster-api-periodics-%s.yaml"
+
+  versions:
+    "1.29":
+      etcd: "3.5.10-0"
+      coreDNS: "v1.11.1"
+      k8sRelease: "stable-1.29"
+    "1.30":
+      etcd: "3.5.10-0"
+      coreDNS: "v1.11.1"
+      k8sRelease: "ci/latest-1.30"
+```
+
+With this configuration, the template `cluster-api-periodics.yaml.tpl` would get executed for each branch.
+In this example we only configure the `main` branch which results in the output file `cluster-api-periodics-main.yaml`.
+
+When executing a template, the following functions are available as addition to the standard functions in go templates:
+
+- `TrimPrefix`: [strings.TrimPrefix](https://pkg.go.dev/strings#TrimPrefix)
+- `TrimSuffix`: [strings.TrimSuffix](https://pkg.go.dev/strings#TrimSuffix)
+- `ReplaceAll`: [strings.ReplaceAll](https://pkg.go.dev/strings#ReplaceAll)
+- `last`: `func(any) any`: returns the last element of an array or slice.
+
+When executing a template, the following variables are available:
+
+- `branch`: The branch name the file get's templated for (The key in `.prow_ignored.branches`).
+- `config`: The branch's configuration from `.prow_ignored.branches.<branch>`.
+- `versions`: The versions mapper from `.prow_ignored.versions`.
diff --git a/hack/tools/prowjob-gen/config.go b/hack/tools/prowjob-gen/config.go
new file mode 100644
index 000000000000..6a083f425262
--- /dev/null
+++ b/hack/tools/prowjob-gen/config.go
@@ -0,0 +1,56 @@
+/*
+Copyright 2024 The Kubernetes Authors.
+
+Licensed 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.
+*/
+
+package main
+
+// ProwIgnoredConfig is the top-level configuration struct. Because we want to
+// store the configuration in test-infra as yaml file, we have to prevent prow
+// from trying to parse our configuration as prow configuration. Prow provides
+// the well-known `prow_ignored` key which is not parsed further by Prow.
+type ProwIgnoredConfig struct {
+	ProwIgnored Config `json:"prow_ignored"`
+}
+
+// Config is the configuration file struct.
+type Config struct {
+	Branches       map[string]BranchConfig `json:"branches"`
+	Templates      []Template              `json:"templates"`
+	VersionsMapper VersionsMapper          `json:"versions"`
+}
+
+// BranchConfig is the branch-based configuration struct.
+type BranchConfig struct {
+	Interval                            string     `json:"interval"`
+	KubekinsImage                       string     `json:"kubekinsImage"`
+	KubernetesVersionManagement         string     `json:"kubernetesVersionManagement"`
+	KubebuilderEnvtestKubernetesVersion string     `json:"kubebuilderEnvtestKubernetesVersion"`
+	Upgrades                            []*Upgrade `json:"upgrades"`
+}
+
+// Template refers a template file and defines the target file name format.
+type Template struct {
+	Format string `json:"format"`
+	Name   string `json:"name"`
+}
+
+// Upgrade describes a kubernetes upgrade.
+type Upgrade struct {
+	From string `json:"from"`
+	To   string `json:"to"`
+}
+
+// VersionsMapper provides key value pairs for a parent key.
+type VersionsMapper map[string]map[string]string
diff --git a/hack/tools/prowjob-gen/generator.go b/hack/tools/prowjob-gen/generator.go
new file mode 100644
index 000000000000..ed2666db06ed
--- /dev/null
+++ b/hack/tools/prowjob-gen/generator.go
@@ -0,0 +1,164 @@
+/*
+Copyright 2024 The Kubernetes Authors.
+
+Licensed 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.
+*/
+
+package main
+
+import (
+	"bytes"
+	"fmt"
+	"os"
+	"path"
+	"path/filepath"
+	"reflect"
+	"strings"
+	"text/template"
+
+	"github.com/pkg/errors"
+	"k8s.io/klog/v2"
+)
+
+const generatedFileHeader = "# Code generated by cluster-api's prowjob-gen. DO NOT EDIT.\n"
+
+// newGenerator initializes a generator which includes parsing the configured templates.
+func newGenerator(config Config, templatesDir, outputDir string) (*generator, error) {
+	g := &generator{
+		config:       config,
+		outputDir:    outputDir,
+		createdFiles: map[string]bool{},
+	}
+
+	var err error
+	g.templates, err = template.New("").
+		Funcs(g.templateFunctions()).
+		ParseGlob(templatesDir + "/*.yaml.tpl")
+	if err != nil {
+		return nil, err
+	}
+
+	return g, err
+}
+
+type generator struct {
+	templates    *template.Template
+	config       Config
+	outputDir    string
+	createdFiles map[string]bool
+}
+
+// generate executes every template for every branch and writes the result to a
+// file in outputDir.
+func (g *generator) generate() error {
+	for _, tpl := range g.config.Templates {
+		for branch := range g.config.Branches {
+			out, err := g.executeTemplate(branch, tpl.Name)
+			if err != nil && !errors.Is(err, os.ErrNotExist) {
+				return errors.Wrapf(err, "Generating prowjobs for template %s", tpl.Name)
+			}
+
+			fileName := fmt.Sprintf(tpl.Format, strings.ReplaceAll(branch, ".", "-"))
+			filePath := filepath.Clean(path.Join(g.outputDir, fileName))
+			if err := os.WriteFile(filePath, out.Bytes(), 0644); err != nil { //nolint:gosec
+				return errors.Wrapf(err, "Writing prowjob to %q", filePath)
+			}
+
+			g.createdFiles[fileName] = true
+		}
+	}
+	return nil
+}
+
+// cleanup deletes files which have the generatedFileHeader and had not been updated
+// during generate.
+func (g *generator) cleanup() error {
+	entries, err := os.ReadDir(g.outputDir)
+	if err != nil {
+		return err
+	}
+
+	for _, entry := range entries {
+		if _, ok := g.createdFiles[entry.Name()]; ok {
+			continue
+		}
+
+		if entry.IsDir() {
+			continue
+		}
+
+		path := filepath.Clean(path.Join(g.outputDir, entry.Name()))
+		data, err := os.ReadFile(path)
+		if err != nil {
+			return err
+		}
+
+		if strings.HasPrefix(string(data), generatedFileHeader) {
+			klog.Infof("Deleting file %s", entry.Name())
+			if err := os.Remove(path); err != nil {
+				return err
+			}
+		}
+	}
+
+	return nil
+}
+
+// executeTemplate executes a previously parsed template with the data for a specific branch.
+func (g *generator) executeTemplate(branch, templateName string) (*bytes.Buffer, error) {
+	klog.Infof("executing template %q for branch %q", templateName, branch)
+
+	data := map[string]interface{}{
+		"branch":   branch,
+		"config":   g.config.Branches[branch],
+		"versions": g.config.VersionsMapper,
+	}
+
+	var out bytes.Buffer
+
+	// Write yaml comment as header to indicate this file got generated.
+	out.WriteString(generatedFileHeader)
+
+	if err := g.templates.ExecuteTemplate(&out, templateName, data); err != nil {
+		return nil, errors.Wrapf(err, "Executing template %q for branch %q", templateName, branch)
+	}
+
+	return &out, nil
+}
+
+// templateFunctions returns the functions available inside of templates.
+func (g *generator) templateFunctions() template.FuncMap {
+	funcs := map[string]any{}
+	funcs["TrimPrefix"] = strings.TrimPrefix
+	funcs["TrimSuffix"] = strings.TrimSuffix
+	funcs["ReplaceAll"] = strings.ReplaceAll
+	funcs["last"] = last
+	return funcs
+}
+
+func last(list any) any {
+	tp := reflect.TypeOf(list).Kind()
+	switch tp {
+	case reflect.Slice, reflect.Array:
+		l2 := reflect.ValueOf(list)
+
+		l := l2.Len()
+		if l == 0 {
+			return nil
+		}
+
+		return l2.Index(l - 1).Interface()
+	default:
+		panic(fmt.Sprintf("Cannot find last on type %s", tp))
+	}
+}
diff --git a/hack/tools/prowjob-gen/main.go b/hack/tools/prowjob-gen/main.go
new file mode 100644
index 000000000000..8f631538d27c
--- /dev/null
+++ b/hack/tools/prowjob-gen/main.go
@@ -0,0 +1,72 @@
+/*
+Copyright 2024 The Kubernetes Authors.
+
+Licensed 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.
+*/
+
+// main is the main package for prowjob-gen.
+package main
+
+import (
+	"flag"
+	"os"
+
+	"k8s.io/klog/v2"
+	"sigs.k8s.io/yaml"
+)
+
+var (
+	configFile   = flag.String("config", "", "Path to the config file")
+	outputDir    = flag.String("output-dir", "", "Path to the directory to create the files in")
+	templatesDir = flag.String("templates-dir", "", "Path to the directory containing the template files referenced inside the config file")
+)
+
+func main() {
+	// Parse flags and validate input.
+	flag.Parse()
+	if *configFile == "" {
+		klog.Fatal("Expected flag \"config\" to be set")
+	}
+	if *outputDir == "" {
+		klog.Fatal("Expected flag \"output-dir\" to be set")
+	}
+	if *templatesDir == "" {
+		klog.Fatal("Expected flag \"templates-dir\" to be set")
+	}
+
+	// Read and Unmarshal the configuration file.
+	rawConfig, err := os.ReadFile(*configFile)
+	if err != nil {
+		klog.Fatalf("Failed to read config file %q: %v", *configFile, err)
+	}
+	prowIgnoredConfig := ProwIgnoredConfig{}
+	if err := yaml.Unmarshal(rawConfig, &prowIgnoredConfig); err != nil {
+		klog.Fatalf("Failed to parse config file %q: %v", *configFile, err)
+	}
+
+	// Initialize a generator using the config data.
+	g, err := newGenerator(prowIgnoredConfig.ProwIgnored, *templatesDir, *outputDir)
+	if err != nil {
+		klog.Fatalf("Failed to initialize generator: %v", err)
+	}
+
+	// Generate new files.
+	if err := g.generate(); err != nil {
+		klog.Fatalf("Failed to generate prowjobs: %v", err)
+	}
+
+	// Cleanup old files which did not get updated.
+	if err := g.cleanup(); err != nil {
+		klog.Fatalf("Failed to cleanup old generated files: %v", err)
+	}
+}
diff --git a/hack/tools/prowjob-gen/main_test.go b/hack/tools/prowjob-gen/main_test.go
new file mode 100644
index 000000000000..a1caaa0be601
--- /dev/null
+++ b/hack/tools/prowjob-gen/main_test.go
@@ -0,0 +1,30 @@
+/*
+Copyright 2024 The Kubernetes Authors.
+
+Licensed 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.
+*/
+
+// main is the main package for prowjob-gen.
+package main
+
+import (
+	"testing"
+)
+
+func Test_newGenerator(t *testing.T) {
+	_, err := newGenerator(Config{}, "test", "")
+	if err != nil {
+		t.Errorf("newGenerator() error = %v", err)
+		return
+	}
+}
diff --git a/hack/tools/prowjob-gen/test/test.yaml.tpl b/hack/tools/prowjob-gen/test/test.yaml.tpl
new file mode 100644
index 000000000000..e69de29bb2d1